diff --git a/components/brave_ads/browser/ads_service_impl.cc b/components/brave_ads/browser/ads_service_impl.cc
index b0334b039565..241decf1d1dd 100644
--- a/components/brave_ads/browser/ads_service_impl.cc
+++ b/components/brave_ads/browser/ads_service_impl.cc
@@ -350,6 +350,7 @@ void AdsServiceImpl::StartBatAdsService() {
   }
 
   bat_ads_service_remote_->Create(
+      ads_service_path_,
       bat_ads_client_associated_receiver_.BindNewEndpointAndPassRemote(),
       bat_ads_associated_remote_.BindNewEndpointAndPassReceiver(),
       std::move(bat_ads_client_notifier_pending_receiver_),
@@ -410,18 +411,9 @@ void AdsServiceImpl::Initialize(const size_t current_start_number) {
     return;
   }
 
-  InitializeDatabase();
-
   InitializeRewardsWallet(current_start_number);
 }
 
-void AdsServiceImpl::InitializeDatabase() {
-  CHECK(!database_);
-
-  database_ = base::SequenceBound<Database>(
-      file_task_runner_, ads_service_path_.AppendASCII(kDatabaseFilename));
-}
-
 void AdsServiceImpl::InitializeRewardsWallet(
     const size_t current_start_number) {
   rewards_service_observation_.GetSource()->GetRewardsWallet(
@@ -1100,8 +1092,6 @@ void AdsServiceImpl::ShutdownAdsService() {
 
   CloseAdaptiveCaptcha();
 
-  database_.Reset();
-
   if (is_bat_ads_initialized_) {
     VLOG(2) << "Shutdown Bat Ads Service";
   }
@@ -1759,17 +1749,6 @@ void AdsServiceImpl::ShowScheduledCaptcha(const std::string& payment_id,
 #endif  // !BUILDFLAG(IS_ANDROID)
 }
 
-void AdsServiceImpl::RunDBTransaction(
-    mojom::DBTransactionInfoPtr mojom_db_transaction,
-    RunDBTransactionCallback callback) {
-  CHECK(mojom_db_transaction);
-  CHECK(database_);
-
-  database_.AsyncCall(&Database::RunDBTransaction)
-      .WithArgs(std::move(mojom_db_transaction))
-      .Then(std::move(callback));
-}
-
 void AdsServiceImpl::RecordP2AEvents(const std::vector<std::string>& events) {
   for (const auto& event : events) {
     RecordAndEmitP2AHistogramName(prefs_,
diff --git a/components/brave_ads/browser/ads_service_impl.h b/components/brave_ads/browser/ads_service_impl.h
index d133be6bfce6..20fb14daaab2 100644
--- a/components/brave_ads/browser/ads_service_impl.h
+++ b/components/brave_ads/browser/ads_service_impl.h
@@ -19,7 +19,6 @@
 #include "base/memory/scoped_refptr.h"
 #include "base/memory/weak_ptr.h"
 #include "base/task/cancelable_task_tracker.h"
-#include "base/threading/sequence_bound.h"
 #include "base/time/time.h"
 #include "base/timer/timer.h"
 #include "brave/components/brave_adaptive_captcha/brave_adaptive_captcha_service.h"
@@ -61,7 +60,6 @@ namespace brave_ads {
 class AdsServiceObserver;
 class AdsTooltipsDelegate;
 class BatAdsServiceFactory;
-class Database;
 class DeviceId;
 class ResourceComponent;
 struct NewTabPageAdInfo;
@@ -127,7 +125,6 @@ class AdsServiceImpl final : public AdsService,
   void InitializeBasePathDirectoryCallback(size_t current_start_number,
                                            bool success);
   void Initialize(size_t current_start_number);
-  void InitializeDatabase();
   void InitializeRewardsWallet(size_t current_start_number);
   void InitializeRewardsWalletCallback(
       size_t current_start_number,
@@ -370,9 +367,6 @@ class AdsServiceImpl final : public AdsService,
   void ShowScheduledCaptcha(const std::string& payment_id,
                             const std::string& captcha_id) override;
 
-  void RunDBTransaction(mojom::DBTransactionInfoPtr mojom_db_transaction,
-                        RunDBTransactionCallback callback) override;
-
   // TODO(https://github.com/brave/brave-browser/issues/14666) Decouple P2A
   // business logic.
   void RecordP2AEvents(const std::vector<std::string>& events) override;
@@ -440,8 +434,6 @@ class AdsServiceImpl final : public AdsService,
 
   mojom::SysInfo sys_info_;
 
-  base::SequenceBound<Database> database_;
-
   base::RepeatingTimer idle_state_timer_;
   ui::IdleState last_idle_state_ = ui::IdleState::IDLE_STATE_ACTIVE;
   base::TimeDelta last_idle_time_;
diff --git a/components/brave_ads/core/internal/BUILD.gn b/components/brave_ads/core/internal/BUILD.gn
index aabac2df6166..befdda93513d 100644
--- a/components/brave_ads/core/internal/BUILD.gn
+++ b/components/brave_ads/core/internal/BUILD.gn
@@ -586,6 +586,7 @@ static_library("internal") {
     "creatives/segments_database_table.h",
     "creatives/segments_database_util.cc",
     "creatives/segments_database_util.h",
+    "database/background_database_handler.cc",
     "database/database.cc",
     "database/database_maintenance.cc",
     "database/database_maintenance.h",
@@ -594,6 +595,8 @@ static_library("internal") {
     "database/database_manager_observer.h",
     "database/database_table_interface.cc",
     "database/database_table_interface.h",
+    "database/test_database_handler.cc",
+    "database/test_database_handler.h",
     "deprecated/client/client_info.cc",
     "deprecated/client/client_info.h",
     "deprecated/client/client_state_manager.cc",
diff --git a/components/brave_ads/core/internal/account/confirmations/queue/confirmation_queue_database_table.cc b/components/brave_ads/core/internal/account/confirmations/queue/confirmation_queue_database_table.cc
index 90da050a848a..137c13de57a2 100644
--- a/components/brave_ads/core/internal/account/confirmations/queue/confirmation_queue_database_table.cc
+++ b/components/brave_ads/core/internal/account/confirmations/queue/confirmation_queue_database_table.cc
@@ -18,7 +18,6 @@
 #include "brave/components/brave_ads/core/internal/account/confirmations/queue/queue_item/confirmation_queue_item_builder_util.h"
 #include "brave/components/brave_ads/core/internal/account/confirmations/queue/queue_item/confirmation_queue_item_util.h"
 #include "brave/components/brave_ads/core/internal/account/confirmations/reward/reward_confirmation_util.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
 #include "brave/components/brave_ads/core/internal/common/challenge_bypass_ristretto/blinded_token.h"
 #include "brave/components/brave_ads/core/internal/common/challenge_bypass_ristretto/public_key.h"
 #include "brave/components/brave_ads/core/internal/common/challenge_bypass_ristretto/token.h"
@@ -33,7 +32,6 @@
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
 #include "brave/components/brave_ads/core/public/account/confirmations/confirmation_type.h"
 #include "brave/components/brave_ads/core/public/ad_units/ad_type.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 
 namespace brave_ads::database::table {
 
@@ -396,9 +394,8 @@ void ConfirmationQueue::GetAll(GetConfirmationQueueCallback callback) const {
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 void ConfirmationQueue::GetNext(GetConfirmationQueueCallback callback) const {
@@ -433,9 +430,8 @@ void ConfirmationQueue::GetNext(GetConfirmationQueueCallback callback) const {
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 std::string ConfirmationQueue::GetTableName() const {
diff --git a/components/brave_ads/core/internal/account/deposits/deposits_database_table.cc b/components/brave_ads/core/internal/account/deposits/deposits_database_table.cc
index aaad8ed72505..0a830b9e9dc3 100644
--- a/components/brave_ads/core/internal/account/deposits/deposits_database_table.cc
+++ b/components/brave_ads/core/internal/account/deposits/deposits_database_table.cc
@@ -11,7 +11,6 @@
 #include "base/check.h"
 #include "base/functional/bind.h"
 #include "base/strings/string_util.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_column_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_statement_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_table_util.h"
@@ -19,7 +18,6 @@
 #include "brave/components/brave_ads/core/internal/common/logging_util.h"
 #include "brave/components/brave_ads/core/internal/common/time/time_util.h"
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 
 namespace brave_ads::database::table {
 
@@ -191,10 +189,9 @@ void Deposits::GetForCreativeInstanceId(const std::string& creative_instance_id,
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetForCreativeInstanceIdCallback, creative_instance_id,
-                     std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetForCreativeInstanceIdCallback,
+                                  creative_instance_id, std::move(callback)));
 }
 
 void Deposits::PurgeExpired(ResultCallback callback) const {
diff --git a/components/brave_ads/core/internal/account/transactions/transactions_database_table.cc b/components/brave_ads/core/internal/account/transactions/transactions_database_table.cc
index 7a0f2e3a9380..2da75e8d15fa 100644
--- a/components/brave_ads/core/internal/account/transactions/transactions_database_table.cc
+++ b/components/brave_ads/core/internal/account/transactions/transactions_database_table.cc
@@ -242,9 +242,8 @@ void Transactions::GetForDateRange(const base::Time from_time,
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 void Transactions::Reconcile(const PaymentTokenList& payment_tokens,
diff --git a/components/brave_ads/core/internal/ads.cc b/components/brave_ads/core/internal/ads.cc
index 8a23294e7054..4cabb81b1976 100644
--- a/components/brave_ads/core/internal/ads.cc
+++ b/components/brave_ads/core/internal/ads.cc
@@ -5,15 +5,21 @@
 
 #include "brave/components/brave_ads/core/public/ads.h"
 
+#include <utility>
+
 #include "brave/components/brave_ads/core/internal/account/tokens/token_generator.h"
 #include "brave/components/brave_ads/core/internal/ads_impl.h"
+#include "brave/components/brave_ads/core/public/database/database_handler_interface.h"
 
 namespace brave_ads {
 
 // static
-std::unique_ptr<Ads> Ads::CreateInstance(AdsClient& ads_client) {
+std::unique_ptr<Ads> Ads::CreateInstance(
+    AdsClient& ads_client,
+    std::unique_ptr<DatabaseHandlerInterface> database_handler) {
   return std::make_unique<AdsImpl>(ads_client,
-                                   std::make_unique<TokenGenerator>());
+                                   std::make_unique<TokenGenerator>(),
+                                   std::move(database_handler));
 }
 
 }  // namespace brave_ads
diff --git a/components/brave_ads/core/internal/ads_client/ads_client_mock.h b/components/brave_ads/core/internal/ads_client/ads_client_mock.h
index 0d12e56d6de0..5be914de3263 100644
--- a/components/brave_ads/core/internal/ads_client/ads_client_mock.h
+++ b/components/brave_ads/core/internal/ads_client/ads_client_mock.h
@@ -90,10 +90,6 @@ class AdsClientMock : public AdsClient {
               ShowScheduledCaptcha,
               (const std::string& payment_id, const std::string& captcha_id));
 
-  MOCK_METHOD(void,
-              RunDBTransaction,
-              (mojom::DBTransactionInfoPtr, RunDBTransactionCallback));
-
   MOCK_METHOD(void, RecordP2AEvents, (const std::vector<std::string>& events));
 
   MOCK_METHOD(bool, FindProfilePref, (const std::string& path), (const));
diff --git a/components/brave_ads/core/internal/ads_impl.cc b/components/brave_ads/core/internal/ads_impl.cc
index 33349fdb58c7..1b14655a27d9 100644
--- a/components/brave_ads/core/internal/ads_impl.cc
+++ b/components/brave_ads/core/internal/ads_impl.cc
@@ -5,6 +5,7 @@
 
 #include "brave/components/brave_ads/core/internal/ads_impl.h"
 
+#include <memory>
 #include <optional>
 #include <utility>
 
@@ -26,6 +27,7 @@
 #include "brave/components/brave_ads/core/internal/legacy_migration/confirmations/legacy_confirmation_migration.h"
 #include "brave/components/brave_ads/core/internal/user_engagement/ad_events/ad_events.h"
 #include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
+#include "brave/components/brave_ads/core/public/database/database_handler_interface.h"
 #include "brave/components/brave_ads/core/public/service/ads_service_callback.h"
 
 namespace brave_ads {
@@ -41,8 +43,11 @@ void FailedToInitialize(InitializeCallback callback) {
 }  // namespace
 
 AdsImpl::AdsImpl(AdsClient& ads_client,
-                 std::unique_ptr<TokenGeneratorInterface> token_generator)
-    : global_state_(ads_client, std::move(token_generator)),
+                 std::unique_ptr<TokenGeneratorInterface> token_generator,
+                 std::unique_ptr<DatabaseHandlerInterface> database_handler)
+    : global_state_(ads_client,
+                    std::move(token_generator),
+                    std::move(database_handler)),
       database_maintenance_(std::make_unique<database::Maintenance>()) {}
 
 AdsImpl::~AdsImpl() = default;
diff --git a/components/brave_ads/core/internal/ads_impl.h b/components/brave_ads/core/internal/ads_impl.h
index 7d9e948aa14e..bc6e1c53fcfd 100644
--- a/components/brave_ads/core/internal/ads_impl.h
+++ b/components/brave_ads/core/internal/ads_impl.h
@@ -32,7 +32,8 @@ class Maintenance;
 class AdsImpl final : public Ads {
  public:
   AdsImpl(AdsClient& ads_client,
-          std::unique_ptr<TokenGeneratorInterface> token_generator);
+          std::unique_ptr<TokenGeneratorInterface> token_generator,
+          std::unique_ptr<DatabaseHandlerInterface> database_handler);
 
   AdsImpl(const AdsImpl&) = delete;
   AdsImpl& operator=(const AdsImpl&) = delete;
diff --git a/components/brave_ads/core/internal/common/database/database_transaction_util.cc b/components/brave_ads/core/internal/common/database/database_transaction_util.cc
index 0f047b7ee5d3..22edbc38e5b3 100644
--- a/components/brave_ads/core/internal/common/database/database_transaction_util.cc
+++ b/components/brave_ads/core/internal/common/database/database_transaction_util.cc
@@ -9,9 +9,10 @@
 
 #include "base/functional/bind.h"
 #include "base/strings/string_util.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
+#include "brave/components/brave_ads/core/internal/database/database_manager.h"
+#include "brave/components/brave_ads/core/internal/global_state/global_state.h"
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
+#include "brave/components/brave_ads/core/public/ads_client/ads_client_callback.h"
 
 namespace brave_ads::database {
 
@@ -43,9 +44,15 @@ bool IsError(
              mojom::DBTransactionResultInfo::StatusCode::kSuccess;
 }
 
+void RunDBTransaction(mojom::DBTransactionInfoPtr mojom_db_transaction,
+                      ::brave_ads::RunDBTransactionCallback callback) {
+  GlobalState::GetInstance()->GetDatabaseManager().RunDBTransaction(
+      std::move(mojom_db_transaction), std::move(callback));
+}
+
 void RunDBTransaction(mojom::DBTransactionInfoPtr mojom_db_transaction,
                       ResultCallback callback) {
-  GetAdsClient().RunDBTransaction(
+  GlobalState::GetInstance()->GetDatabaseManager().RunDBTransaction(
       std::move(mojom_db_transaction),
       base::BindOnce(&RunDBTransactionCallback, std::move(callback)));
 }
diff --git a/components/brave_ads/core/internal/common/database/database_transaction_util.h b/components/brave_ads/core/internal/common/database/database_transaction_util.h
index 8d34e50aabc5..ba1705afcba3 100644
--- a/components/brave_ads/core/internal/common/database/database_transaction_util.h
+++ b/components/brave_ads/core/internal/common/database/database_transaction_util.h
@@ -22,6 +22,11 @@ bool IsSuccess(
 bool IsError(
     const mojom::DBTransactionResultInfoPtr& mojom_db_transaction_result);
 
+// Run a database transaction. The callback takes one argument -
+// `mojom::DBTransactionResultInfoPtr` containing the info of the transaction.
+void RunDBTransaction(mojom::DBTransactionInfoPtr mojom_db_transaction,
+                      RunDBTransactionCallback callback);
+
 // Run a database transaction.
 void RunDBTransaction(mojom::DBTransactionInfoPtr mojom_db_transaction,
                       ResultCallback callback);
diff --git a/components/brave_ads/core/internal/common/test/internal/mock_test_util_internal.cc b/components/brave_ads/core/internal/common/test/internal/mock_test_util_internal.cc
index 8d0e92621c20..0dd65504d559 100644
--- a/components/brave_ads/core/internal/common/test/internal/mock_test_util_internal.cc
+++ b/components/brave_ads/core/internal/common/test/internal/mock_test_util_internal.cc
@@ -224,20 +224,6 @@ void MockLoadDataResource(AdsClientMock& ads_client_mock) {
           }));
 }
 
-void MockRunDBTransaction(AdsClientMock& ads_client_mock, Database& database) {
-  ON_CALL(ads_client_mock, RunDBTransaction)
-      .WillByDefault(::testing::Invoke(
-          [&database](mojom::DBTransactionInfoPtr mojom_db_transaction,
-                      RunDBTransactionCallback callback) {
-            CHECK(mojom_db_transaction);
-
-            mojom::DBTransactionResultInfoPtr mojom_db_transaction_result =
-                database.RunDBTransaction(std::move(mojom_db_transaction));
-
-            std::move(callback).Run(std::move(mojom_db_transaction_result));
-          }));
-}
-
 void MockFindProfilePref(const AdsClientMock& ads_client_mock) {
   ON_CALL(ads_client_mock, FindProfilePref)
       .WillByDefault(::testing::Invoke([](const std::string& path) -> bool {
diff --git a/components/brave_ads/core/internal/common/test/internal/mock_test_util_internal.h b/components/brave_ads/core/internal/common/test/internal/mock_test_util_internal.h
index 9218b670affd..5909648584a9 100644
--- a/components/brave_ads/core/internal/common/test/internal/mock_test_util_internal.h
+++ b/components/brave_ads/core/internal/common/test/internal/mock_test_util_internal.h
@@ -37,8 +37,6 @@ void MockLoadResourceComponent(AdsClientMock& ads_client_mock,
 
 void MockLoadDataResource(AdsClientMock& ads_client_mock);
 
-void MockRunDBTransaction(AdsClientMock& ads_client_mock, Database& database);
-
 void MockFindProfilePref(const AdsClientMock& ads_client_mock);
 void MockGetProfilePref(const AdsClientMock& ads_client_mock);
 void MockSetProfilePref(const AdsClientMock& ads_client_mock,
diff --git a/components/brave_ads/core/internal/common/test/test_base.cc b/components/brave_ads/core/internal/common/test/test_base.cc
index 6642dabfa75f..7f53383622f5 100644
--- a/components/brave_ads/core/internal/common/test/test_base.cc
+++ b/components/brave_ads/core/internal/common/test/test_base.cc
@@ -27,12 +27,12 @@
 #include "brave/components/brave_ads/core/internal/common/test/test_types.h"
 #include "brave/components/brave_ads/core/internal/common/test/time_test_util.h"
 #include "brave/components/brave_ads/core/internal/database/database_manager.h"
+#include "brave/components/brave_ads/core/internal/database/test_database_handler.h"
 #include "brave/components/brave_ads/core/internal/deprecated/client/client_state_manager.h"
 #include "brave/components/brave_ads/core/internal/deprecated/confirmations/confirmation_state_manager.h"
 #include "brave/components/brave_ads/core/internal/global_state/global_state.h"
 #include "brave/components/brave_ads/core/public/ads.h"
 #include "brave/components/brave_ads/core/public/ads_constants.h"
-#include "brave/components/brave_ads/core/public/database/database.h"
 
 namespace brave_ads::test {
 
@@ -238,10 +238,6 @@ void TestBase::MockAdsClient() {
 
   MockLoadDataResource(ads_client_mock_);
 
-  database_ =
-      std::make_unique<Database>(ProfilePath().AppendASCII(kDatabaseFilename));
-  MockRunDBTransaction(ads_client_mock_, *database_);
-
   MockFindProfilePref(ads_client_mock_);
   MockGetProfilePref(ads_client_mock_);
   MockSetProfilePref(ads_client_mock_, *this);
@@ -302,7 +298,9 @@ void TestBase::SetUpIntegrationTest() {
       << "SetUpIntegrationTest should only be called if SetUp is initialized "
          "for integration testing";
 
-  ads_ = Ads::CreateInstance(ads_client_mock_);
+  ads_ = Ads::CreateInstance(ads_client_mock_,
+                             std::make_unique<TestDatabaseHandler>(
+                                 ProfilePath().AppendASCII(kDatabaseFilename)));
   CHECK(ads_) << "Failed to create ads instance";
 
   // Must be called after `Ads` is instantiated but prior to `Initialize`.
@@ -332,7 +330,9 @@ void TestBase::SetUpUnitTest() {
                                   "SetUp is initialized for unit testing";
 
   global_state_ = std::make_unique<GlobalState>(
-      ads_client_mock_, std::make_unique<TokenGeneratorMock>());
+      ads_client_mock_, std::make_unique<TokenGeneratorMock>(),
+      std::make_unique<TestDatabaseHandler>(
+          ProfilePath().AppendASCII(kDatabaseFilename)));
 
   // Must be called after `GlobalState` is instantiated but prior to
   // `MockDefaultAdsServiceState`.
diff --git a/components/brave_ads/core/internal/creatives/conversions/creative_set_conversion_database_table.cc b/components/brave_ads/core/internal/creatives/conversions/creative_set_conversion_database_table.cc
index 8a2e4c78bfe2..4b9e00b8ac84 100644
--- a/components/brave_ads/core/internal/creatives/conversions/creative_set_conversion_database_table.cc
+++ b/components/brave_ads/core/internal/creatives/conversions/creative_set_conversion_database_table.cc
@@ -23,7 +23,6 @@
 #include "brave/components/brave_ads/core/internal/common/time/time_util.h"
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
 #include "brave/components/brave_ads/core/public/account/confirmations/confirmation_type.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 
 namespace brave_ads::database::table {
 
@@ -220,9 +219,8 @@ void CreativeSetConversions::GetUnexpired(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 void CreativeSetConversions::GetActive(
@@ -252,9 +250,8 @@ void CreativeSetConversions::GetActive(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 void CreativeSetConversions::PurgeExpired(ResultCallback callback) const {
diff --git a/components/brave_ads/core/internal/creatives/creative_ads_database_table.cc b/components/brave_ads/core/internal/creatives/creative_ads_database_table.cc
index 1703459c221b..16daddf03520 100644
--- a/components/brave_ads/core/internal/creatives/creative_ads_database_table.cc
+++ b/components/brave_ads/core/internal/creatives/creative_ads_database_table.cc
@@ -14,13 +14,11 @@
 #include "base/functional/bind.h"
 #include "base/strings/strcat.h"
 #include "base/strings/string_util.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_column_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_table_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_transaction_util.h"
 #include "brave/components/brave_ads/core/internal/common/logging_util.h"
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 #include "url/gurl.h"
 
 namespace brave_ads::database::table {
@@ -218,10 +216,9 @@ void CreativeAds::GetForCreativeInstanceId(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetForCreativeInstanceIdCallback, creative_instance_id,
-                     std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetForCreativeInstanceIdCallback,
+                                  creative_instance_id, std::move(callback)));
 }
 
 std::string CreativeAds::GetTableName() const {
diff --git a/components/brave_ads/core/internal/creatives/inline_content_ads/creative_inline_content_ads_database_table.cc b/components/brave_ads/core/internal/creatives/inline_content_ads/creative_inline_content_ads_database_table.cc
index a666eb079072..46841e4908f8 100644
--- a/components/brave_ads/core/internal/creatives/inline_content_ads/creative_inline_content_ads_database_table.cc
+++ b/components/brave_ads/core/internal/creatives/inline_content_ads/creative_inline_content_ads_database_table.cc
@@ -15,7 +15,6 @@
 #include "base/strings/strcat.h"
 #include "base/strings/string_util.h"
 #include "base/time/time.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
 #include "brave/components/brave_ads/core/internal/common/containers/container_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_column_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_statement_util.h"
@@ -26,7 +25,6 @@
 #include "brave/components/brave_ads/core/internal/creatives/creative_ad_info.h"
 #include "brave/components/brave_ads/core/internal/segments/segment_util.h"
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 #include "url/gurl.h"
 
 namespace brave_ads::database::table {
@@ -353,10 +351,9 @@ void CreativeInlineContentAds::GetForCreativeInstanceId(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetForCreativeInstanceIdCallback, creative_instance_id,
-                     std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetForCreativeInstanceIdCallback,
+                                  creative_instance_id, std::move(callback)));
 }
 
 void CreativeInlineContentAds::GetForSegmentsAndDimensions(
@@ -425,10 +422,9 @@ void CreativeInlineContentAds::GetForSegmentsAndDimensions(
 
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetForSegmentsAndDimensionsCallback, segments,
-                     std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetForSegmentsAndDimensionsCallback,
+                                  segments, std::move(callback)));
 }
 
 void CreativeInlineContentAds::GetForDimensions(
@@ -486,7 +482,7 @@ void CreativeInlineContentAds::GetForDimensions(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
+  RunDBTransaction(
       std::move(mojom_db_transaction),
       base::BindOnce(&GetForDimensionsCallback, std::move(callback)));
 }
@@ -539,9 +535,8 @@ void CreativeInlineContentAds::GetForActiveCampaigns(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetAllCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetAllCallback, std::move(callback)));
 }
 
 std::string CreativeInlineContentAds::GetTableName() const {
diff --git a/components/brave_ads/core/internal/creatives/new_tab_page_ads/creative_new_tab_page_ads_database_table.cc b/components/brave_ads/core/internal/creatives/new_tab_page_ads/creative_new_tab_page_ads_database_table.cc
index b8d0c048c44e..6524ae164563 100644
--- a/components/brave_ads/core/internal/creatives/new_tab_page_ads/creative_new_tab_page_ads_database_table.cc
+++ b/components/brave_ads/core/internal/creatives/new_tab_page_ads/creative_new_tab_page_ads_database_table.cc
@@ -15,7 +15,6 @@
 #include "base/strings/strcat.h"
 #include "base/strings/string_split.h"
 #include "base/time/time.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
 #include "brave/components/brave_ads/core/internal/common/containers/container_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_column_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_statement_util.h"
@@ -26,7 +25,6 @@
 #include "brave/components/brave_ads/core/internal/creatives/creative_ad_info.h"
 #include "brave/components/brave_ads/core/internal/segments/segment_util.h"
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 #include "brave/components/brave_ads/core/public/serving/targeting/condition_matcher/condition_matcher_util.h"
 #include "url/gurl.h"
 
@@ -391,10 +389,9 @@ void CreativeNewTabPageAds::GetForCreativeInstanceId(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetForCreativeInstanceIdCallback, creative_instance_id,
-                     std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetForCreativeInstanceIdCallback,
+                                  creative_instance_id, std::move(callback)));
 }
 
 void CreativeNewTabPageAds::GetForSegments(
@@ -464,7 +461,7 @@ void CreativeNewTabPageAds::GetForSegments(
 
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
+  RunDBTransaction(
       std::move(mojom_db_transaction),
       base::BindOnce(&GetForSegmentsCallback, segments, std::move(callback)));
 }
@@ -520,9 +517,8 @@ void CreativeNewTabPageAds::GetForActiveCampaigns(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetAllCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetAllCallback, std::move(callback)));
 }
 
 std::string CreativeNewTabPageAds::GetTableName() const {
diff --git a/components/brave_ads/core/internal/creatives/notification_ads/creative_notification_ads_database_table.cc b/components/brave_ads/core/internal/creatives/notification_ads/creative_notification_ads_database_table.cc
index b8b4b8059a1f..a324c78a740b 100644
--- a/components/brave_ads/core/internal/creatives/notification_ads/creative_notification_ads_database_table.cc
+++ b/components/brave_ads/core/internal/creatives/notification_ads/creative_notification_ads_database_table.cc
@@ -14,7 +14,6 @@
 #include "base/strings/strcat.h"
 #include "base/strings/string_util.h"
 #include "base/time/time.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
 #include "brave/components/brave_ads/core/internal/common/containers/container_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_column_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_statement_util.h"
@@ -25,7 +24,6 @@
 #include "brave/components/brave_ads/core/internal/creatives/creative_ad_info.h"
 #include "brave/components/brave_ads/core/internal/segments/segment_util.h"
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 #include "url/gurl.h"
 
 namespace brave_ads::database::table {
@@ -310,7 +308,7 @@ void CreativeNotificationAds::GetForSegments(
 
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
+  RunDBTransaction(
       std::move(mojom_db_transaction),
       base::BindOnce(&GetForSegmentsCallback, segments, std::move(callback)));
 }
@@ -360,9 +358,8 @@ void CreativeNotificationAds::GetForActiveCampaigns(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetAllCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetAllCallback, std::move(callback)));
 }
 
 std::string CreativeNotificationAds::GetTableName() const {
diff --git a/components/brave_ads/core/internal/creatives/promoted_content_ads/creative_promoted_content_ads_database_table.cc b/components/brave_ads/core/internal/creatives/promoted_content_ads/creative_promoted_content_ads_database_table.cc
index 6d79890904f9..249733e24a36 100644
--- a/components/brave_ads/core/internal/creatives/promoted_content_ads/creative_promoted_content_ads_database_table.cc
+++ b/components/brave_ads/core/internal/creatives/promoted_content_ads/creative_promoted_content_ads_database_table.cc
@@ -14,7 +14,6 @@
 #include "base/strings/strcat.h"
 #include "base/strings/string_util.h"
 #include "base/time/time.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
 #include "brave/components/brave_ads/core/internal/common/containers/container_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_column_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_statement_util.h"
@@ -25,7 +24,6 @@
 #include "brave/components/brave_ads/core/internal/creatives/creative_ad_info.h"
 #include "brave/components/brave_ads/core/internal/segments/segment_util.h"
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 #include "url/gurl.h"
 
 namespace brave_ads::database::table {
@@ -326,10 +324,9 @@ void CreativePromotedContentAds::GetForCreativeInstanceId(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetForCreativeInstanceIdCallback, creative_instance_id,
-                     std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetForCreativeInstanceIdCallback,
+                                  creative_instance_id, std::move(callback)));
 }
 
 void CreativePromotedContentAds::GetForSegments(
@@ -394,7 +391,7 @@ void CreativePromotedContentAds::GetForSegments(
 
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
+  RunDBTransaction(
       std::move(mojom_db_transaction),
       base::BindOnce(&GetForSegmentsCallback, segments, std::move(callback)));
 }
@@ -444,9 +441,8 @@ void CreativePromotedContentAds::GetForActiveCampaigns(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetAllCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetAllCallback, std::move(callback)));
 }
 
 std::string CreativePromotedContentAds::GetTableName() const {
diff --git a/components/brave_ads/core/internal/database/background_database_handler.cc b/components/brave_ads/core/internal/database/background_database_handler.cc
new file mode 100644
index 000000000000..5489c2b0eade
--- /dev/null
+++ b/components/brave_ads/core/internal/database/background_database_handler.cc
@@ -0,0 +1,39 @@
+/* Copyright (c) 2024 The Brave Authors. All rights reserved.
+ * This Source Code Form is subject to the terms of the Mozilla Public
+ * License, v. 2.0. If a copy of the MPL was not distributed with this file,
+ * You can obtain one at https://mozilla.org/MPL/2.0/. */
+
+#include "brave/components/brave_ads/core/public/database/background_database_handler.h"
+
+#include <utility>
+
+#include "base/check.h"
+#include "base/task/task_traits.h"
+#include "base/task/thread_pool.h"
+#include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
+#include "brave/components/brave_ads/core/public/database/database.h"
+
+namespace brave_ads {
+
+BackgroundDatabaseHandler::BackgroundDatabaseHandler(
+    const base::FilePath& database_path)
+    : database_task_runner_(base::ThreadPool::CreateSequencedTaskRunner(
+          {base::MayBlock(), base::TaskPriority::BEST_EFFORT,
+           base::TaskShutdownBehavior::BLOCK_SHUTDOWN})),
+      database_(base::SequenceBound<Database>(database_task_runner_,
+                                              database_path)) {}
+
+BackgroundDatabaseHandler::~BackgroundDatabaseHandler() = default;
+
+void BackgroundDatabaseHandler::RunDBTransaction(
+    mojom::DBTransactionInfoPtr mojom_db_transaction,
+    RunDBTransactionCallback callback) {
+  CHECK(mojom_db_transaction);
+  CHECK(database_);
+
+  database_.AsyncCall(&Database::RunDBTransaction)
+      .WithArgs(std::move(mojom_db_transaction))
+      .Then(std::move(callback));
+}
+
+}  // namespace brave_ads
diff --git a/components/brave_ads/core/internal/database/database_manager.cc b/components/brave_ads/core/internal/database/database_manager.cc
index 1c9e2ea66d29..f0e6ae5ecbe3 100644
--- a/components/brave_ads/core/internal/database/database_manager.cc
+++ b/components/brave_ads/core/internal/database/database_manager.cc
@@ -5,12 +5,12 @@
 
 #include "brave/components/brave_ads/core/internal/database/database_manager.h"
 
+#include <memory>
 #include <utility>
 
 #include "base/check_op.h"
 #include "base/debug/dump_without_crashing.h"
 #include "base/functional/bind.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_transaction_util.h"
 #include "brave/components/brave_ads/core/internal/common/logging_util.h"
 #include "brave/components/brave_ads/core/internal/global_state/global_state.h"
@@ -19,11 +19,13 @@
 #include "brave/components/brave_ads/core/internal/legacy_migration/database/database_migration.h"
 #include "brave/components/brave_ads/core/internal/legacy_migration/database/database_raze.h"
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
+#include "brave/components/brave_ads/core/public/database/database_handler_interface.h"
 
 namespace brave_ads {
 
-DatabaseManager::DatabaseManager() = default;
+DatabaseManager::DatabaseManager(
+    std::unique_ptr<DatabaseHandlerInterface> database_handler)
+    : database_handler_(std::move(database_handler)) {}
 
 DatabaseManager::~DatabaseManager() = default;
 
@@ -53,12 +55,22 @@ void DatabaseManager::CreateOrOpen(ResultCallback callback) {
   mojom_db_action->type = mojom::DBActionInfo::Type::kInitialize;
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
+  RunDBTransaction(
       std::move(mojom_db_transaction),
       base::BindOnce(&DatabaseManager::CreateOrOpenCallback,
                      weak_factory_.GetWeakPtr(), std::move(callback)));
 }
 
+void DatabaseManager::RunDBTransaction(
+    mojom::DBTransactionInfoPtr mojom_db_transaction,
+    RunDBTransactionCallback callback) {
+  CHECK(mojom_db_transaction);
+  CHECK(database_handler_);
+
+  database_handler_->RunDBTransaction(std::move(mojom_db_transaction),
+                                      std::move(callback));
+}
+
 ///////////////////////////////////////////////////////////////////////////////
 
 void DatabaseManager::CreateOrOpenCallback(
diff --git a/components/brave_ads/core/internal/database/database_manager.h b/components/brave_ads/core/internal/database/database_manager.h
index a2f33715739f..9f8fc4fed20e 100644
--- a/components/brave_ads/core/internal/database/database_manager.h
+++ b/components/brave_ads/core/internal/database/database_manager.h
@@ -6,16 +6,22 @@
 #ifndef BRAVE_COMPONENTS_BRAVE_ADS_CORE_INTERNAL_DATABASE_DATABASE_MANAGER_H_
 #define BRAVE_COMPONENTS_BRAVE_ADS_CORE_INTERNAL_DATABASE_DATABASE_MANAGER_H_
 
+#include <memory>
+
 #include "base/memory/weak_ptr.h"
 #include "base/observer_list.h"
 #include "brave/components/brave_ads/core/internal/database/database_manager_observer.h"
+#include "brave/components/brave_ads/core/mojom/brave_ads.mojom-forward.h"
 #include "brave/components/brave_ads/core/public/ads_client/ads_client_callback.h"
 
 namespace brave_ads {
 
+class DatabaseHandlerInterface;
+
 class DatabaseManager final {
  public:
-  DatabaseManager();
+  explicit DatabaseManager(
+      std::unique_ptr<DatabaseHandlerInterface> database_handler);
 
   DatabaseManager(const DatabaseManager&) = delete;
   DatabaseManager& operator=(const DatabaseManager&) = delete;
@@ -33,6 +39,11 @@ class DatabaseManager final {
   // Create or open the database.
   void CreateOrOpen(ResultCallback callback);
 
+  // Run a database transaction. The callback takes one argument -
+  // `mojom::DBTransactionResultInfoPtr` containing the info of the transaction.
+  void RunDBTransaction(mojom::DBTransactionInfoPtr mojom_db_transaction,
+                        RunDBTransactionCallback callback);
+
  private:
   void CreateOrOpenCallback(
       ResultCallback callback,
@@ -63,6 +74,8 @@ class DatabaseManager final {
   void NotifyFailedToMigrateDatabase(int from_version, int to_version) const;
   void NotifyDatabaseIsReady() const;
 
+  const std::unique_ptr<DatabaseHandlerInterface> database_handler_;
+
   base::ObserverList<DatabaseManagerObserver> observers_;
 
   base::WeakPtrFactory<DatabaseManager> weak_factory_{this};
diff --git a/components/brave_ads/core/internal/database/test_database_handler.cc b/components/brave_ads/core/internal/database/test_database_handler.cc
new file mode 100644
index 000000000000..2111843b03c6
--- /dev/null
+++ b/components/brave_ads/core/internal/database/test_database_handler.cc
@@ -0,0 +1,32 @@
+/* Copyright (c) 2024 The Brave Authors. All rights reserved.
+ * This Source Code Form is subject to the terms of the Mozilla Public
+ * License, v. 2.0. If a copy of the MPL was not distributed with this file,
+ * You can obtain one at https://mozilla.org/MPL/2.0/. */
+
+#include "brave/components/brave_ads/core/internal/database/test_database_handler.h"
+
+#include <utility>
+
+#include "base/check.h"
+#include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
+#include "brave/components/brave_ads/core/public/database/database.h"
+
+namespace brave_ads::test {
+
+TestDatabaseHandler::TestDatabaseHandler(const base::FilePath& database_path)
+    : database_(database_path) {}
+
+TestDatabaseHandler::~TestDatabaseHandler() = default;
+
+void TestDatabaseHandler::RunDBTransaction(
+    mojom::DBTransactionInfoPtr mojom_db_transaction,
+    RunDBTransactionCallback callback) {
+  CHECK(mojom_db_transaction);
+
+  mojom::DBTransactionResultInfoPtr mojom_db_transaction_result =
+      database_.RunDBTransaction(std::move(mojom_db_transaction));
+
+  std::move(callback).Run(std::move(mojom_db_transaction_result));
+}
+
+}  // namespace brave_ads::test
diff --git a/components/brave_ads/core/internal/database/test_database_handler.h b/components/brave_ads/core/internal/database/test_database_handler.h
new file mode 100644
index 000000000000..47906a365da8
--- /dev/null
+++ b/components/brave_ads/core/internal/database/test_database_handler.h
@@ -0,0 +1,37 @@
+/* Copyright (c) 2024 The Brave Authors. All rights reserved.
+ * This Source Code Form is subject to the terms of the Mozilla Public
+ * License, v. 2.0. If a copy of the MPL was not distributed with this file,
+ * You can obtain one at https://mozilla.org/MPL/2.0/. */
+
+#ifndef BRAVE_COMPONENTS_BRAVE_ADS_CORE_INTERNAL_DATABASE_TEST_DATABASE_HANDLER_H_
+#define BRAVE_COMPONENTS_BRAVE_ADS_CORE_INTERNAL_DATABASE_TEST_DATABASE_HANDLER_H_
+
+#include "brave/components/brave_ads/core/mojom/brave_ads.mojom-forward.h"
+#include "brave/components/brave_ads/core/public/ads_client/ads_client_callback.h"
+#include "brave/components/brave_ads/core/public/database/database.h"
+#include "brave/components/brave_ads/core/public/database/database_handler_interface.h"
+
+namespace brave_ads::test {
+
+class TestDatabaseHandler : public DatabaseHandlerInterface {
+ public:
+  explicit TestDatabaseHandler(const base::FilePath& database_path);
+
+  TestDatabaseHandler(const TestDatabaseHandler&) = delete;
+  TestDatabaseHandler& operator=(const TestDatabaseHandler&) = delete;
+
+  TestDatabaseHandler(TestDatabaseHandler&&) noexcept = delete;
+  TestDatabaseHandler& operator=(TestDatabaseHandler&&) noexcept = delete;
+
+  ~TestDatabaseHandler() override;
+
+  void RunDBTransaction(mojom::DBTransactionInfoPtr mojom_db_transaction,
+                        RunDBTransactionCallback callback) override;
+
+ private:
+  Database database_;
+};
+
+}  // namespace brave_ads::test
+
+#endif  // BRAVE_COMPONENTS_BRAVE_ADS_CORE_INTERNAL_DATABASE_TEST_DATABASE_HANDLER_H_
diff --git a/components/brave_ads/core/internal/global_state/global_state.cc b/components/brave_ads/core/internal/global_state/global_state.cc
index 57f93ceb808b..64a4b55bad22 100644
--- a/components/brave_ads/core/internal/global_state/global_state.cc
+++ b/components/brave_ads/core/internal/global_state/global_state.cc
@@ -23,19 +23,22 @@
 #include "brave/components/brave_ads/core/internal/tabs/tab_manager.h"
 #include "brave/components/brave_ads/core/internal/user_attention/user_activity/user_activity_manager.h"
 #include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
+#include "brave/components/brave_ads/core/public/database/database_handler_interface.h"
 
 namespace brave_ads {
 
 GlobalState::GlobalState(
     AdsClient& ads_client,
-    std::unique_ptr<TokenGeneratorInterface> token_generator)
+    std::unique_ptr<TokenGeneratorInterface> token_generator,
+    std::unique_ptr<DatabaseHandlerInterface> database_handler)
     : ads_client_(ads_client),
       global_state_holder_(std::make_unique<GlobalStateHolder>(this)) {
   ads_notifier_manager_ = std::make_unique<AdsNotifierManager>();
   browser_manager_ = std::make_unique<BrowserManager>();
   client_state_manager_ = std::make_unique<ClientStateManager>();
   confirmation_state_manager_ = std::make_unique<ConfirmationStateManager>();
-  database_manager_ = std::make_unique<DatabaseManager>();
+  database_manager_ =
+      std::make_unique<DatabaseManager>(std::move(database_handler));
   diagnostic_manager_ = std::make_unique<DiagnosticManager>();
   ad_history_manager_ = std::make_unique<AdHistoryManager>();
   notification_ad_manager_ = std::make_unique<NotificationAdManager>();
diff --git a/components/brave_ads/core/internal/global_state/global_state.h b/components/brave_ads/core/internal/global_state/global_state.h
index 09cf350da87b..1f2cfbb30f08 100644
--- a/components/brave_ads/core/internal/global_state/global_state.h
+++ b/components/brave_ads/core/internal/global_state/global_state.h
@@ -25,6 +25,7 @@ class AdsNotifierManager;
 class BrowserManager;
 class ClientStateManager;
 class ConfirmationStateManager;
+class DatabaseHandlerInterface;
 class DatabaseManager;
 class DiagnosticManager;
 class GlobalStateHolder;
@@ -35,9 +36,9 @@ class UserActivityManager;
 
 class GlobalState final {
  public:
-  explicit GlobalState(
-      AdsClient& ads_client,
-      std::unique_ptr<TokenGeneratorInterface> token_generator);
+  GlobalState(AdsClient& ads_client,
+              std::unique_ptr<TokenGeneratorInterface> token_generator,
+              std::unique_ptr<DatabaseHandlerInterface> database_handler);
 
   GlobalState(const GlobalState& other) = delete;
   GlobalState& operator=(const GlobalState& other) = delete;
diff --git a/components/brave_ads/core/internal/history/ad_history_database_table.cc b/components/brave_ads/core/internal/history/ad_history_database_table.cc
index e0a20250fc6f..e15786251275 100644
--- a/components/brave_ads/core/internal/history/ad_history_database_table.cc
+++ b/components/brave_ads/core/internal/history/ad_history_database_table.cc
@@ -12,7 +12,6 @@
 #include "base/debug/dump_without_crashing.h"
 #include "base/strings/string_util.h"
 #include "base/time/time.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
 #include "brave/components/brave_ads/core/internal/common/containers/container_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_column_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_statement_util.h"
@@ -23,7 +22,6 @@
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
 #include "brave/components/brave_ads/core/public/account/confirmations/confirmation_type.h"
 #include "brave/components/brave_ads/core/public/ad_units/ad_type.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 #include "brave/components/brave_ads/core/public/history/ad_history_feature.h"
 
 namespace brave_ads::database::table {
@@ -265,9 +263,8 @@ void AdHistory::GetForDateRange(const base::Time from_time,
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 void AdHistory::GetHighestRankedPlacementsForDateRange(
@@ -369,9 +366,8 @@ void AdHistory::GetHighestRankedPlacementsForDateRange(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 void AdHistory::GetForCreativeInstanceId(
@@ -404,9 +400,8 @@ void AdHistory::GetForCreativeInstanceId(
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 void AdHistory::PurgeExpired(ResultCallback callback) const {
diff --git a/components/brave_ads/core/internal/user_engagement/ad_events/ad_events_database_table.cc b/components/brave_ads/core/internal/user_engagement/ad_events/ad_events_database_table.cc
index ad3fb277783a..c7bbd4ad11dc 100644
--- a/components/brave_ads/core/internal/user_engagement/ad_events/ad_events_database_table.cc
+++ b/components/brave_ads/core/internal/user_engagement/ad_events/ad_events_database_table.cc
@@ -11,7 +11,6 @@
 #include "base/check.h"
 #include "base/functional/bind.h"
 #include "base/strings/string_util.h"
-#include "brave/components/brave_ads/core/internal/ads_client/ads_client_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_column_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_statement_util.h"
 #include "brave/components/brave_ads/core/internal/common/database/database_table_util.h"
@@ -22,7 +21,6 @@
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom.h"
 #include "brave/components/brave_ads/core/public/account/confirmations/confirmation_type.h"
 #include "brave/components/brave_ads/core/public/ad_units/ad_type.h"
-#include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 
 namespace brave_ads::database::table {
 
@@ -205,9 +203,8 @@ void AdEvents::GetAll(GetAdEventsCallback callback) const {
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 void AdEvents::GetUnexpired(GetAdEventsCallback callback) const {
@@ -245,9 +242,8 @@ void AdEvents::GetUnexpired(GetAdEventsCallback callback) const {
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 void AdEvents::GetUnexpired(const mojom::AdType mojom_ad_type,
@@ -289,9 +285,8 @@ void AdEvents::GetUnexpired(const mojom::AdType mojom_ad_type,
   BindColumnTypes(mojom_db_action);
   mojom_db_transaction->actions.push_back(std::move(mojom_db_action));
 
-  GetAdsClient().RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(&GetCallback, std::move(callback)));
+  RunDBTransaction(std::move(mojom_db_transaction),
+                   base::BindOnce(&GetCallback, std::move(callback)));
 }
 
 void AdEvents::PurgeExpired(ResultCallback callback) const {
diff --git a/components/brave_ads/core/public/BUILD.gn b/components/brave_ads/core/public/BUILD.gn
index 56182e38b5a9..56a21fc1600d 100644
--- a/components/brave_ads/core/public/BUILD.gn
+++ b/components/brave_ads/core/public/BUILD.gn
@@ -31,7 +31,9 @@ source_set("headers") {
     "ads_feature.h",
     "ads_observer_interface.h",
     "ads_util.h",
+    "database/background_database_handler.h",
     "database/database.h",
+    "database/database_handler_interface.h",
     "export.h",
     "flags/flags_util.h",
     "history/ad_history_feature.h",
diff --git a/components/brave_ads/core/public/ads.h b/components/brave_ads/core/public/ads.h
index c7fecc71668a..8ee23b7e2144 100644
--- a/components/brave_ads/core/public/ads.h
+++ b/components/brave_ads/core/public/ads.h
@@ -22,6 +22,7 @@ class Time;
 namespace brave_ads {
 
 class AdsClient;
+class DatabaseHandlerInterface;
 struct NotificationAdInfo;
 
 class ADS_EXPORT Ads {
@@ -36,7 +37,9 @@ class ADS_EXPORT Ads {
 
   virtual ~Ads() = default;
 
-  static std::unique_ptr<Ads> CreateInstance(AdsClient& ads_client);
+  static std::unique_ptr<Ads> CreateInstance(
+      AdsClient& ads_client,
+      std::unique_ptr<DatabaseHandlerInterface> database_handler);
 
   virtual void AddObserver(
       std::unique_ptr<AdsObserverInterface> ads_observer) = 0;
diff --git a/components/brave_ads/core/public/ads_client/ads_client.h b/components/brave_ads/core/public/ads_client/ads_client.h
index 8b502d425483..9fb73c92d585 100644
--- a/components/brave_ads/core/public/ads_client/ads_client.h
+++ b/components/brave_ads/core/public/ads_client/ads_client.h
@@ -115,12 +115,6 @@ class ADS_EXPORT AdsClient {
   virtual void ShowScheduledCaptcha(const std::string& payment_id,
                                     const std::string& captcha_id) = 0;
 
-  // Run a database transaction. The callback takes one argument -
-  // `mojom::DBTransactionResultInfoPtr` containing the info of the transaction.
-  virtual void RunDBTransaction(
-      mojom::DBTransactionInfoPtr mojom_db_transaction,
-      RunDBTransactionCallback callback) = 0;
-
   // Record P2A (Private Advertising Analytics) `events`.
   virtual void RecordP2AEvents(const std::vector<std::string>& events) = 0;
 
diff --git a/components/brave_ads/core/public/database/background_database_handler.h b/components/brave_ads/core/public/database/background_database_handler.h
new file mode 100644
index 000000000000..9e388ba99d5f
--- /dev/null
+++ b/components/brave_ads/core/public/database/background_database_handler.h
@@ -0,0 +1,45 @@
+/* Copyright (c) 2024 The Brave Authors. All rights reserved.
+ * This Source Code Form is subject to the terms of the Mozilla Public
+ * License, v. 2.0. If a copy of the MPL was not distributed with this file,
+ * You can obtain one at https://mozilla.org/MPL/2.0/. */
+
+#ifndef BRAVE_COMPONENTS_BRAVE_ADS_CORE_PUBLIC_DATABASE_BACKGROUND_DATABASE_HANDLER_H_
+#define BRAVE_COMPONENTS_BRAVE_ADS_CORE_PUBLIC_DATABASE_BACKGROUND_DATABASE_HANDLER_H_
+
+#include "base/task/sequenced_task_runner.h"
+#include "base/threading/sequence_bound.h"
+#include "brave/components/brave_ads/core/mojom/brave_ads.mojom-forward.h"
+#include "brave/components/brave_ads/core/public/ads_client/ads_client_callback.h"
+#include "brave/components/brave_ads/core/public/database/database.h"
+#include "brave/components/brave_ads/core/public/database/database_handler_interface.h"
+
+namespace brave_ads {
+
+class Database;
+
+class BackgroundDatabaseHandler : public DatabaseHandlerInterface {
+ public:
+  explicit BackgroundDatabaseHandler(const base::FilePath& database_path);
+
+  BackgroundDatabaseHandler(const BackgroundDatabaseHandler&) = delete;
+  BackgroundDatabaseHandler& operator=(const BackgroundDatabaseHandler&) =
+      delete;
+
+  BackgroundDatabaseHandler(BackgroundDatabaseHandler&&) noexcept = delete;
+  BackgroundDatabaseHandler& operator=(BackgroundDatabaseHandler&&) noexcept =
+      delete;
+
+  ~BackgroundDatabaseHandler() override;
+
+  void RunDBTransaction(mojom::DBTransactionInfoPtr mojom_db_transaction,
+                        RunDBTransactionCallback callback) override;
+
+ private:
+  const scoped_refptr<base::SequencedTaskRunner> database_task_runner_;
+
+  const base::SequenceBound<Database> database_;
+};
+
+}  // namespace brave_ads
+
+#endif  // BRAVE_COMPONENTS_BRAVE_ADS_CORE_PUBLIC_DATABASE_BACKGROUND_DATABASE_HANDLER_H_
diff --git a/components/brave_ads/core/public/database/database_handler_interface.h b/components/brave_ads/core/public/database/database_handler_interface.h
new file mode 100644
index 000000000000..f0034622ad74
--- /dev/null
+++ b/components/brave_ads/core/public/database/database_handler_interface.h
@@ -0,0 +1,25 @@
+/* Copyright (c) 2024 The Brave Authors. All rights reserved.
+ * This Source Code Form is subject to the terms of the Mozilla Public
+ * License, v. 2.0. If a copy of the MPL was not distributed with this file,
+ * You can obtain one at https://mozilla.org/MPL/2.0/. */
+
+#ifndef BRAVE_COMPONENTS_BRAVE_ADS_CORE_PUBLIC_DATABASE_DATABASE_HANDLER_INTERFACE_H_
+#define BRAVE_COMPONENTS_BRAVE_ADS_CORE_PUBLIC_DATABASE_DATABASE_HANDLER_INTERFACE_H_
+
+#include "brave/components/brave_ads/core/mojom/brave_ads.mojom-forward.h"
+#include "brave/components/brave_ads/core/public/ads_client/ads_client_callback.h"
+
+namespace brave_ads {
+
+class DatabaseHandlerInterface {
+ public:
+  virtual ~DatabaseHandlerInterface() = default;
+
+  virtual void RunDBTransaction(
+      mojom::DBTransactionInfoPtr mojom_db_transaction,
+      RunDBTransactionCallback callback) = 0;
+};
+
+}  // namespace brave_ads
+
+#endif  // BRAVE_COMPONENTS_BRAVE_ADS_CORE_PUBLIC_DATABASE_DATABASE_HANDLER_INTERFACE_H_
diff --git a/components/services/bat_ads/bat_ads_client_mojo_bridge.cc b/components/services/bat_ads/bat_ads_client_mojo_bridge.cc
index 2369ebb1a513..c5e29f17f380 100644
--- a/components/services/bat_ads/bat_ads_client_mojo_bridge.cc
+++ b/components/services/bat_ads/bat_ads_client_mojo_bridge.cc
@@ -241,18 +241,6 @@ std::string BatAdsClientMojoBridge::LoadDataResource(const std::string& name) {
   return value;
 }
 
-void BatAdsClientMojoBridge::RunDBTransaction(
-    brave_ads::mojom::DBTransactionInfoPtr mojom_db_transaction,
-    brave_ads::RunDBTransactionCallback callback) {
-  if (!bat_ads_client_associated_remote_.is_bound()) {
-    std::move(callback).Run(brave_ads::mojom::DBTransactionResultInfoPtr());
-    return;
-  }
-
-  bat_ads_client_associated_remote_->RunDBTransaction(
-      std::move(mojom_db_transaction), std::move(callback));
-}
-
 void BatAdsClientMojoBridge::ShowScheduledCaptcha(
     const std::string& payment_id,
     const std::string& captcha_id) {
diff --git a/components/services/bat_ads/bat_ads_client_mojo_bridge.h b/components/services/bat_ads/bat_ads_client_mojo_bridge.h
index 49ebc02c5a86..0ccc3c662636 100644
--- a/components/services/bat_ads/bat_ads_client_mojo_bridge.h
+++ b/components/services/bat_ads/bat_ads_client_mojo_bridge.h
@@ -94,10 +94,6 @@ class BatAdsClientMojoBridge : public brave_ads::AdsClient {
   void ShowScheduledCaptcha(const std::string& payment_id,
                             const std::string& captcha_id) override;
 
-  void RunDBTransaction(
-      brave_ads::mojom::DBTransactionInfoPtr mojom_db_transaction,
-      brave_ads::RunDBTransactionCallback callback) override;
-
   void RecordP2AEvents(const std::vector<std::string>& events) override;
 
   bool FindProfilePref(const std::string& path) const override;
diff --git a/components/services/bat_ads/bat_ads_impl.cc b/components/services/bat_ads/bat_ads_impl.cc
index 26f4e14b5ab2..91531fb85cc0 100644
--- a/components/services/bat_ads/bat_ads_impl.cc
+++ b/components/services/bat_ads/bat_ads_impl.cc
@@ -18,7 +18,9 @@
 #include "brave/components/brave_ads/core/public/ad_units/notification_ad/notification_ad_info.h"
 #include "brave/components/brave_ads/core/public/ad_units/notification_ad/notification_ad_value_util.h"
 #include "brave/components/brave_ads/core/public/ads.h"
+#include "brave/components/brave_ads/core/public/ads_constants.h"
 #include "brave/components/brave_ads/core/public/ads_observer_interface.h"
+#include "brave/components/brave_ads/core/public/database/background_database_handler.h"
 #include "brave/components/services/bat_ads/bat_ads_client_mojo_bridge.h"
 #include "brave/components/services/bat_ads/bat_ads_observer.h"
 
@@ -27,13 +29,17 @@ namespace bat_ads {
 class BatAdsImpl::AdsInstance final {
  public:
   AdsInstance(
+      const base::FilePath& service_path,
       mojo::PendingAssociatedRemote<mojom::BatAdsClient>
           bat_ads_client_pending_associated_remote,
       mojo::PendingReceiver<mojom::BatAdsClientNotifier> client_notifier)
       : bat_ads_client_mojo_proxy_(std::make_unique<BatAdsClientMojoBridge>(
             std::move(bat_ads_client_pending_associated_remote),
             std::move(client_notifier))),
-        ads_(brave_ads::Ads::CreateInstance(*bat_ads_client_mojo_proxy_)) {}
+        ads_(brave_ads::Ads::CreateInstance(
+            *bat_ads_client_mojo_proxy_,
+            std::make_unique<brave_ads::BackgroundDatabaseHandler>(
+                service_path.AppendASCII(brave_ads::kDatabaseFilename)))) {}
 
   AdsInstance(const AdsInstance&) = delete;
   AdsInstance& operator=(const AdsInstance&) = delete;
@@ -50,12 +56,14 @@ class BatAdsImpl::AdsInstance final {
   std::unique_ptr<brave_ads::Ads> ads_;
 };
 
-BatAdsImpl::BatAdsImpl(mojo::PendingAssociatedRemote<mojom::BatAdsClient>
+BatAdsImpl::BatAdsImpl(const base::FilePath& service_path,
+                       mojo::PendingAssociatedRemote<mojom::BatAdsClient>
                            bat_ads_client_pending_associated_remote,
                        mojo::PendingReceiver<mojom::BatAdsClientNotifier>
                            bat_ads_client_notifier_pending_receiver)
     : ads_instance_(std::unique_ptr<AdsInstance, base::OnTaskRunnerDeleter>(
-          new AdsInstance(std::move(bat_ads_client_pending_associated_remote),
+          new AdsInstance(service_path,
+                          std::move(bat_ads_client_pending_associated_remote),
                           std::move(bat_ads_client_notifier_pending_receiver)),
           base::OnTaskRunnerDeleter(
               base::SequencedTaskRunner::GetCurrentDefault()))) {}
diff --git a/components/services/bat_ads/bat_ads_impl.h b/components/services/bat_ads/bat_ads_impl.h
index 2fbb639cf2c1..502d27f25113 100644
--- a/components/services/bat_ads/bat_ads_impl.h
+++ b/components/services/bat_ads/bat_ads_impl.h
@@ -25,7 +25,8 @@ class BatAdsClientMojoBridge;
 
 class BatAdsImpl : public mojom::BatAds {
  public:
-  BatAdsImpl(mojo::PendingAssociatedRemote<mojom::BatAdsClient>
+  BatAdsImpl(const base::FilePath& service_path,
+             mojo::PendingAssociatedRemote<mojom::BatAdsClient>
                  bat_ads_client_pending_associated_remote,
              mojo::PendingReceiver<mojom::BatAdsClientNotifier>
                  bat_ads_client_notifier_pending_receiver);
diff --git a/components/services/bat_ads/bat_ads_service_impl.cc b/components/services/bat_ads/bat_ads_service_impl.cc
index e583ec2572a6..0faf10cfd212 100644
--- a/components/services/bat_ads/bat_ads_service_impl.cc
+++ b/components/services/bat_ads/bat_ads_service_impl.cc
@@ -8,6 +8,7 @@
 #include <memory>
 #include <utility>
 
+#include "base/files/file_path.h"
 #include "brave/components/services/bat_ads/bat_ads_impl.h"
 #include "brave/components/services/bat_ads/public/interfaces/bat_ads.mojom.h"
 #include "mojo/public/cpp/bindings/sync_call_restrictions.h"
@@ -33,6 +34,7 @@ BatAdsServiceImpl::BatAdsServiceImpl(mojo::PendingReceiver<mojom::BatAdsService>
 BatAdsServiceImpl::~BatAdsServiceImpl() = default;
 
 void BatAdsServiceImpl::Create(
+    const base::FilePath& service_path,
     mojo::PendingAssociatedRemote<mojom::BatAdsClient>
         bat_ads_client_pending_associated_remote,
     mojo::PendingAssociatedReceiver<mojom::BatAds>
@@ -44,7 +46,7 @@ void BatAdsServiceImpl::Create(
 
   bat_ads_associated_receivers_.Add(
       std::make_unique<BatAdsImpl>(
-          std::move(bat_ads_client_pending_associated_remote),
+          service_path, std::move(bat_ads_client_pending_associated_remote),
           std::move(bat_ads_client_notifier_pending_receiver)),
       std::move(bat_ads_pending_associated_receiver));
 
diff --git a/components/services/bat_ads/bat_ads_service_impl.h b/components/services/bat_ads/bat_ads_service_impl.h
index bc530fbf5907..bec5e2fc5486 100644
--- a/components/services/bat_ads/bat_ads_service_impl.h
+++ b/components/services/bat_ads/bat_ads_service_impl.h
@@ -35,7 +35,8 @@ class BatAdsServiceImpl : public mojom::BatAdsService {
   ~BatAdsServiceImpl() override;
 
   // BatAdsService:
-  void Create(mojo::PendingAssociatedRemote<mojom::BatAdsClient>
+  void Create(const base::FilePath& service_path,
+              mojo::PendingAssociatedRemote<mojom::BatAdsClient>
                   bat_ads_client_pending_associated_remote,
               mojo::PendingAssociatedReceiver<mojom::BatAds>
                   bat_ads_pending_associated_receiver,
diff --git a/components/services/bat_ads/public/interfaces/bat_ads.mojom b/components/services/bat_ads/public/interfaces/bat_ads.mojom
index 3ced4e7089ef..331fd69815cf 100644
--- a/components/services/bat_ads/public/interfaces/bat_ads.mojom
+++ b/components/services/bat_ads/public/interfaces/bat_ads.mojom
@@ -7,12 +7,14 @@ module bat_ads.mojom;
 import "brave/components/brave_ads/core/mojom/brave_ads.mojom";
 import "mojo/public/mojom/base/big_string.mojom";
 import "mojo/public/mojom/base/file.mojom";
+import "mojo/public/mojom/base/file_path.mojom";
 import "mojo/public/mojom/base/time.mojom";
 import "mojo/public/mojom/base/values.mojom";
 import "url/mojom/url.mojom";
 
 interface BatAdsService {
-  Create(pending_associated_remote<BatAdsClient>
+  Create(mojo_base.mojom.FilePath service_path,
+         pending_associated_remote<BatAdsClient>
              bat_ads_client_pending_associated_remote,
          pending_associated_receiver<BatAds>
              bat_ads_pending_associated_receiver,
@@ -111,9 +113,6 @@ interface BatAdsClient {
 
   ShowScheduledCaptcha(string payment_id, string captcha_id);
 
-  RunDBTransaction(brave_ads.mojom.DBTransactionInfo mojom_db_transaction) =>
-      (brave_ads.mojom.DBTransactionResultInfo mojom_db_transaction_result);
-
   RecordP2AEvents(array<string> events);
 
   [Sync]
diff --git a/ios/browser/api/ads/ads_client_bridge.h b/ios/browser/api/ads/ads_client_bridge.h
index f559ff705e09..5bdbfc843412 100644
--- a/ios/browser/api/ads/ads_client_bridge.h
+++ b/ios/browser/api/ads/ads_client_bridge.h
@@ -59,9 +59,6 @@
 - (void)resetAdEventCacheForInstanceId:(const std::string&)id;
 - (void)UrlRequest:(brave_ads::mojom::UrlRequestInfoPtr)url_request
           callback:(brave_ads::UrlRequestCallback)callback;
-- (void)runDBTransaction:
-            (brave_ads::mojom::DBTransactionInfoPtr)mojom_db_transaction
-                callback:(brave_ads::RunDBTransactionCallback)callback;
 - (void)setProfilePref:(const std::string&)path value:(base::Value)value;
 - (bool)findProfilePref:(const std::string&)path;
 - (std::optional<base::Value>)getProfilePref:(const std::string&)path;
diff --git a/ios/browser/api/ads/ads_client_ios.h b/ios/browser/api/ads/ads_client_ios.h
index 381a74ec3cc9..c9c87b7914a9 100644
--- a/ios/browser/api/ads/ads_client_ios.h
+++ b/ios/browser/api/ads/ads_client_ios.h
@@ -64,9 +64,6 @@ class AdsClientIOS : public brave_ads::AdsClient {
            const int line,
            const int verbose_level,
            const std::string& message) override;
-  void RunDBTransaction(
-      brave_ads::mojom::DBTransactionInfoPtr mojom_db_transaction,
-      brave_ads::RunDBTransactionCallback callback) override;
   void SetProfilePref(const std::string& path, base::Value value) override;
   bool FindProfilePref(const std::string& path) const override;
   std::optional<base::Value> GetProfilePref(const std::string& path) override;
diff --git a/ios/browser/api/ads/ads_client_ios.mm b/ios/browser/api/ads/ads_client_ios.mm
index 7eddfc0d0b8a..87b7c1073162 100644
--- a/ios/browser/api/ads/ads_client_ios.mm
+++ b/ios/browser/api/ads/ads_client_ios.mm
@@ -135,13 +135,6 @@
   [bridge_ log:file line:line verboseLevel:verbose_level message:message];
 }
 
-void AdsClientIOS::RunDBTransaction(
-    brave_ads::mojom::DBTransactionInfoPtr mojom_db_transaction,
-    brave_ads::RunDBTransactionCallback callback) {
-  [bridge_ runDBTransaction:std::move(mojom_db_transaction)
-                   callback:std::move(callback)];
-}
-
 void AdsClientIOS::SetProfilePref(const std::string& path, base::Value value) {
   [bridge_ setProfilePref:path value:std::move(value)];
 }
diff --git a/ios/browser/api/ads/brave_ads.mm b/ios/browser/api/ads/brave_ads.mm
index 2e79d72d853b..e1292b051fee 100644
--- a/ios/browser/api/ads/brave_ads.mm
+++ b/ios/browser/api/ads/brave_ads.mm
@@ -1407,25 +1407,6 @@ - (void)showScheduledCaptcha:(const std::string&)payment_id
                               captchaId:base::SysUTF8ToNSString(captcha_id)];
 }
 
-- (void)runDBTransaction:
-            (brave_ads::mojom::DBTransactionInfoPtr)mojom_db_transaction
-                callback:(brave_ads::RunDBTransactionCallback)completion {
-  if (![self isServiceRunning]) {
-    return std::move(completion)
-        .Run(brave_ads::mojom::DBTransactionResultInfo::New());
-  }
-
-  adsService->RunDBTransaction(
-      std::move(mojom_db_transaction),
-      base::BindOnce(
-          ^(brave_ads::RunDBTransactionCallback callback,
-            brave_ads::mojom::DBTransactionResultInfoPtr
-                mojom_db_transaction_result) {
-            std::move(callback).Run(std::move(mojom_db_transaction_result));
-          },
-          std::move(completion)));
-}
-
 - (void)recordP2AEvents:(const std::vector<std::string>&)events {
   // TODO(https://github.com/brave/brave-browser/issues/33786): Unify Brave Ads
   // P3A analytics.
diff --git a/ios/browser/brave_ads/ads_service_impl_ios.h b/ios/browser/brave_ads/ads_service_impl_ios.h
index a60310981de4..3b828d2a131f 100644
--- a/ios/browser/brave_ads/ads_service_impl_ios.h
+++ b/ios/browser/brave_ads/ads_service_impl_ios.h
@@ -11,7 +11,6 @@
 #include <vector>
 
 #include "base/memory/weak_ptr.h"
-#include "base/threading/sequence_bound.h"
 #include "brave/components/brave_ads/core/browser/service/ads_service.h"
 #include "brave/components/brave_ads/core/mojom/brave_ads.mojom-forward.h"
 #include "brave/components/brave_ads/core/public/ads_callback.h"
@@ -28,7 +27,6 @@ namespace brave_ads {
 
 class Ads;
 class AdsClient;
-class Database;
 
 class AdsServiceImplIOS : public AdsService {
  public:
@@ -166,7 +164,6 @@ class AdsServiceImplIOS : public AdsService {
 
   void InitializeAds(InitializeCallback callback);
   void InitializeAdsCallback(InitializeCallback callback, bool success);
-  void InitializeDatabase();
 
   void ShutdownAdsCallback(ShutdownCallback callback, bool success);
 
@@ -175,7 +172,7 @@ class AdsServiceImplIOS : public AdsService {
 
   const raw_ptr<PrefService> prefs_ = nullptr;  // Not owned.
 
-  const scoped_refptr<base::SequencedTaskRunner> database_queue_;
+  const scoped_refptr<base::SequencedTaskRunner> file_task_runner_;
 
   base::FilePath storage_path_;
   std::unique_ptr<AdsClient> ads_client_;
@@ -183,8 +180,6 @@ class AdsServiceImplIOS : public AdsService {
   mojom::BuildChannelInfoPtr mojom_build_channel_;
   mojom::WalletInfoPtr mojom_wallet_;
 
-  base::SequenceBound<Database> database_;
-
   std::unique_ptr<Ads> ads_;
 
   base::WeakPtrFactory<AdsServiceImplIOS> weak_ptr_factory_{this};
diff --git a/ios/browser/brave_ads/ads_service_impl_ios.mm b/ios/browser/brave_ads/ads_service_impl_ios.mm
index f30dabbac47a..7ba1cc3edc15 100644
--- a/ios/browser/brave_ads/ads_service_impl_ios.mm
+++ b/ios/browser/brave_ads/ads_service_impl_ios.mm
@@ -23,7 +23,7 @@
 #include "brave/components/brave_ads/core/public/ads.h"
 #include "brave/components/brave_ads/core/public/ads_client/ads_client.h"
 #include "brave/components/brave_ads/core/public/ads_constants.h"
-#include "brave/components/brave_ads/core/public/database/database.h"
+#include "brave/components/brave_ads/core/public/database/background_database_handler.h"
 #include "brave/components/brave_ads/core/public/flags/flags_util.h"
 #include "components/prefs/pref_service.h"
 #include "sql/database.h"
@@ -40,7 +40,7 @@
 AdsServiceImplIOS::AdsServiceImplIOS(PrefService* prefs)
     : AdsService(/*delegate=*/nullptr),
       prefs_(prefs),
-      database_queue_(base::ThreadPool::CreateSequencedTaskRunner(
+      file_task_runner_(base::ThreadPool::CreateSequencedTaskRunner(
           {base::MayBlock(), base::TaskPriority::USER_VISIBLE,
            base::TaskShutdownBehavior::BLOCK_SHUTDOWN})) {
   CHECK(prefs_);
@@ -82,14 +82,6 @@
                                 std::move(callback)));
 }
 
-void AdsServiceImplIOS::RunDBTransaction(
-    mojom::DBTransactionInfoPtr mojom_db_transaction,
-    RunDBTransactionCallback callback) {
-  database_.AsyncCall(&brave_ads::Database::RunDBTransaction)
-      .WithArgs(std::move(mojom_db_transaction))
-      .Then(std::move(callback));
-}
-
 void AdsServiceImplIOS::MaybeGetNotificationAd(
     const std::string& placement_id,
     MaybeGetNotificationAdCallback callback) {
@@ -442,15 +434,14 @@
 
 void AdsServiceImplIOS::Shutdown() {
   ads_.reset();
-  database_.Reset();
 }
 
 void AdsServiceImplIOS::InitializeAds(InitializeCallback callback) {
   CHECK(!IsInitialized());
 
-  InitializeDatabase();
-
-  ads_ = Ads::CreateInstance(*ads_client_);
+  ads_ = Ads::CreateInstance(
+      *ads_client_, std::make_unique<BackgroundDatabaseHandler>(
+                        storage_path_.AppendASCII(kAdsDatabaseFilename)));
 
   ads_->SetSysInfo(mojom_sys_info_.Clone());
   ads_->SetBuildChannel(mojom_build_channel_.Clone());
@@ -471,12 +462,6 @@
   std::move(callback).Run(success);
 }
 
-void AdsServiceImplIOS::InitializeDatabase() {
-  database_ = base::SequenceBound<brave_ads::Database>(
-      database_queue_,
-      base::FilePath(storage_path_.Append(kAdsDatabaseFilename)));
-}
-
 void AdsServiceImplIOS::ShutdownAdsCallback(ShutdownCallback callback,
                                             const bool success) {
   Shutdown();
@@ -495,7 +480,7 @@
     return std::move(callback).Run(/*success=*/false);
   }
 
-  database_queue_->PostTaskAndReply(
+  file_task_runner_->PostTaskAndReply(
       FROM_HERE,
       base::BindOnce(
           [](const base::FilePath& storage_path) {