diff --git a/tool/tsh/common/db.go b/tool/tsh/common/db.go
index c5e033dbb4776..f4a5903532549 100644
--- a/tool/tsh/common/db.go
+++ b/tool/tsh/common/db.go
@@ -44,8 +44,6 @@ import (
 	"github.com/gravitational/teleport/api/types"
 	apiutils "github.com/gravitational/teleport/api/utils"
 	"github.com/gravitational/teleport/api/utils/keys"
-	"github.com/gravitational/teleport/api/utils/prompt"
-	"github.com/gravitational/teleport/lib/auth"
 	"github.com/gravitational/teleport/lib/client"
 	dbprofile "github.com/gravitational/teleport/lib/client/db"
 	"github.com/gravitational/teleport/lib/client/db/dbcmd"
@@ -818,7 +816,7 @@ func onDatabaseConnect(cf *CLIConf) error {
 	return nil
 }
 
-func accessRequestForDB(cf *CLIConf, tc *client.TeleportClient, db types.Database) error {
+func makeAccessRequestForDatabase(tc *client.TeleportClient, db types.Database) (types.AccessRequest, error) {
 	requestResourceIDs := []types.ResourceID{{
 		ClusterName: tc.SiteName,
 		Kind:        types.KindDatabase,
@@ -826,52 +824,42 @@ func accessRequestForDB(cf *CLIConf, tc *client.TeleportClient, db types.Databas
 	}}
 
 	req, err := services.NewAccessRequestWithResources(tc.Username, nil /* roles */, requestResourceIDs)
+	return req, trace.Wrap(err)
+}
+
+func makeDatabaseAccessRequestAndWaitForApproval(cf *CLIConf, tc *client.TeleportClient, db types.Database) error {
+	req, err := makeAccessRequestForDatabase(tc, db)
 	if err != nil {
 		return trace.Wrap(err)
 	}
 
-	cf.RequestID = req.GetName()
-
 	fmt.Fprintf(cf.Stdout(), "You do not currently have access to %q, attempting to request access.\n\n", db.GetName())
-
-	// Prompt for a request reason.
-	requestReason, err := prompt.Input(cf.Context, cf.Stdout(), prompt.Stdin(), "Enter request reason")
-	if err != nil {
+	if err := setAccessRequestReason(cf, req); err != nil {
 		return trace.Wrap(err)
 	}
-	req.SetRequestReason(requestReason)
-
-	fmt.Fprint(os.Stdout, "Creating request...\n")
-	// Always create access request against the root cluster.
-	if err := tc.WithRootClusterClient(cf.Context, func(clt auth.ClientI) error {
-		req, err = clt.CreateAccessRequestV2(cf.Context, req)
-		return trace.Wrap(err)
-	}); err != nil {
+	if err := sendAccessRequestAndWaitForApproval(cf, tc, req); err != nil {
 		return trace.Wrap(err)
 	}
+	return nil
+}
 
-	if cf.Username == "" {
-		cf.Username = tc.Username
-	}
-	// re-fetch the request to display it with roles populated.
-	onRequestShow(cf)
-	fmt.Println("")
+var dbCommandsWithAccessRequestSupport = []string{
+	"db login",
+	"proxy db",
+	"db connect",
+}
 
-	// Wait for the request to be resolved.
-	fmt.Fprintf(os.Stdout, "Waiting for request approval...\n")
-	var resolvedReq types.AccessRequest
-	if err := tc.WithRootClusterClient(cf.Context, func(clt auth.ClientI) error {
-		resolvedReq, err = awaitRequestResolution(cf.Context, clt, req)
-		return trace.Wrap(err)
-	}); err != nil {
-		return trace.Wrap(err)
+func shouldRetryGetDatabaseUsingSearchAsRoles(cf *CLIConf, tc *client.TeleportClient, getDatabaseError error) bool {
+	// Only retry when the database cannot be found without UseSearchAsRoles.
+	if !trace.IsNotFound(getDatabaseError) || tc.UseSearchAsRoles {
+		return false
 	}
-
-	// Handle resolution and update client certs if approved.
-	if err := onRequestResolution(cf, tc, resolvedReq); err != nil {
-		return trace.Wrap(err)
+	// Check if auto access request is disabled.
+	if cf.disableAccessRequest {
+		return false
 	}
-	return nil
+	// Check if the `tsh` command supports auto access request.
+	return slices.Contains(dbCommandsWithAccessRequestSupport, cf.command)
 }
 
 // getDatabaseInfo fetches information about the database from tsh profile if DB
@@ -890,20 +878,32 @@ func getDatabaseInfo(cf *CLIConf, tc *client.TeleportClient, routes []tlsca.Rout
 
 	db, err := getDatabaseByNameOrDiscoveredName(cf, tc, routes)
 	switch {
-	case trace.IsNotFound(err) && !cf.disableAccessRequest && !tc.UseSearchAsRoles:
-		// Try again with SearchAsRoles. TODO optimize to not do
-		// UseSearchAsRoles for "regular" users.
-		tc.UseSearchAsRoles = true
-		searchAsRolesDB, searchAsRolesErr := getDatabaseByNameOrDiscoveredName(cf, tc, nil)
-		if searchAsRolesErr != nil {
-			return nil, trace.Wrap(err)
+	// If the database cannot be found, try again with UseSearchAsRoles. If
+	// the database is then found with UseSearchAsRoles, make an access request
+	// for it and elevate the user with the request ID upon approval.
+	//
+	// Note that the access request must be made before the database connection
+	// is made to avoid mangling the request with the database client tools.
+	// Thus the flow for auto database access request is different from SSH.
+	//
+	// Performance considerations:
+	// - For common scenarios where UseSearchAsRoles is not desired, it would
+	//   be rare that cf.DatabaseName would be not found in the first API call
+	//   so there won't be a second call usually.
+	// - accessChecker.GetAllowedSearchAsRoles can be checked to avoid the
+	//   second API call but creating the access checker requires more calls.
+	// - The db commands do provide "--disable-access-request" to bypass the
+	//   second call. If needed, we can add it to `tsh login` and profile yaml
+	//   in the future.
+	case shouldRetryGetDatabaseUsingSearchAsRoles(cf, tc, err):
+		orgErr := err
+		if db, err = getDatabaseByNameOrDiscoveredNameUsingSearchAsRoles(cf, tc); err != nil {
+			return nil, trace.Wrap(orgErr) // Returns the original not found error.
 		}
-
-		if err := accessRequestForDB(cf, tc, searchAsRolesDB); err != nil {
+		if err := makeDatabaseAccessRequestAndWaitForApproval(cf, tc, db); err != nil {
 			return nil, trace.Wrap(err)
 		}
-
-		db = searchAsRolesDB
+		routes = nil // reset routes after reissueWithRequests.
 
 	case err != nil:
 		return nil, trace.Wrap(err)
@@ -1117,6 +1117,15 @@ func getDatabaseByNameOrDiscoveredName(cf *CLIConf, tc *client.TeleportClient, a
 	return chooseOneDatabase(cf, databases)
 }
 
+func getDatabaseByNameOrDiscoveredNameUsingSearchAsRoles(cf *CLIConf, tc *client.TeleportClient) (types.Database, error) {
+	tc.UseSearchAsRoles = true
+	defer func() {
+		tc.UseSearchAsRoles = false
+	}()
+	db, err := getDatabaseByNameOrDiscoveredName(cf, tc, nil)
+	return db, trace.Wrap(err)
+}
+
 func filterActiveDatabases(routes []tlsca.RouteToDatabase, databases types.Databases) types.Databases {
 	databasesByName := databases.ToMap()
 	var out types.Databases
diff --git a/tool/tsh/common/db_test.go b/tool/tsh/common/db_test.go
index cbe13d26c232a..c6e6c1988e1b7 100644
--- a/tool/tsh/common/db_test.go
+++ b/tool/tsh/common/db_test.go
@@ -62,6 +62,7 @@ func TestTshDB(t *testing.T) {
 	t.Run("Login", testDatabaseLogin)
 	t.Run("List", testListDatabase)
 	t.Run("DatabaseSelection", testDatabaseSelection)
+	t.Run("access request", testDatabaseAccessRequest)
 }
 
 // testDatabaseLogin tests "tsh db login" command and verifies "tsh db
@@ -1758,3 +1759,7 @@ func testDatabaseSelection(t *testing.T) {
 		}
 	})
 }
+
+func testDatabaseAccessRequest(t *testing.T) {
+	// TODO
+}
diff --git a/tool/tsh/common/tsh.go b/tool/tsh/common/tsh.go
index 024149d15a5e9..74661b8163040 100644
--- a/tool/tsh/common/tsh.go
+++ b/tool/tsh/common/tsh.go
@@ -841,6 +841,8 @@ func Run(ctx context.Context, args []string, opts ...CliOption) error {
 	proxyDB.Flag("cluster", clusterHelp).Short('c').StringVar(&cf.SiteName)
 	proxyDB.Flag("labels", labelHelp).StringVar(&cf.Labels)
 	proxyDB.Flag("query", queryHelp).StringVar(&cf.PredicateExpression)
+	proxyDB.Flag("request-reason", "Reason for requesting access").StringVar(&cf.RequestReason)
+	proxyDB.Flag("disable-access-request", "Disable automatic resource access requests").BoolVar(&cf.disableAccessRequest)
 
 	proxyApp := proxy.Command("app", "Start local TLS proxy for app connection when using Teleport in single-port mode.")
 	proxyApp.Arg("app", "The name of the application to start local proxy for").Required().StringVar(&cf.AppName)
@@ -884,6 +886,8 @@ func Run(ctx context.Context, args []string, opts ...CliOption) error {
 	dbLogin.Flag("db-user", "Database user to configure as default.").Short('u').StringVar(&cf.DatabaseUser)
 	dbLogin.Flag("db-name", "Database name to configure as default.").Short('n').StringVar(&cf.DatabaseName)
 	dbLogin.Flag("db-roles", "List of comma separate database roles to use for auto-provisioned user.").Short('r').StringVar(&cf.DatabaseRoles)
+	dbLogin.Flag("request-reason", "Reason for requesting access").StringVar(&cf.RequestReason)
+	dbLogin.Flag("disable-access-request", "Disable automatic resource access requests").BoolVar(&cf.disableAccessRequest)
 	dbLogout := db.Command("logout", "Remove database credentials.")
 	dbLogout.Arg("db", "Database to remove credentials for.").StringVar(&cf.DatabaseService)
 	dbLogout.Flag("labels", labelHelp).StringVar(&cf.Labels)
@@ -910,6 +914,8 @@ func Run(ctx context.Context, args []string, opts ...CliOption) error {
 	dbConnect.Flag("db-roles", "List of comma separate database roles to use for auto-provisioned user.").Short('r').StringVar(&cf.DatabaseRoles)
 	dbConnect.Flag("labels", labelHelp).StringVar(&cf.Labels)
 	dbConnect.Flag("query", queryHelp).StringVar(&cf.PredicateExpression)
+	dbConnect.Flag("request-reason", "Reason for requesting access").StringVar(&cf.RequestReason)
+	dbConnect.Flag("disable-access-request", "Disable automatic resource access requests").BoolVar(&cf.disableAccessRequest)
 
 	// join
 	join := app.Command("join", "Join the active SSH or Kubernetes session.")
@@ -3267,12 +3273,25 @@ func retryWithAccessRequest(
 		log.Debugf("Not attempting to automatically request access, reason: %v", err)
 		return trace.Wrap(origErr)
 	}
-	cf.RequestID = req.GetName()
 
 	// Print and log the original AccessDenied error.
 	fmt.Fprintln(os.Stderr, utils.UserMessageFromError(origErr))
 	fmt.Fprintf(os.Stdout, "You do not currently have access to %q, attempting to request access.\n\n", resource)
 
+	if err := setAccessRequestReason(cf, req); err != nil {
+		return trace.Wrap(err)
+	}
+	if err := sendAccessRequestAndWaitForApproval(cf, tc, req); err != nil {
+		return trace.Wrap(err)
+	}
+
+	// Retry now that request has been approved and certs updated.
+	// Clear the original exit status.
+	tc.ExitStatus = 0
+	return trace.Wrap(fn())
+}
+
+func setAccessRequestReason(cf *CLIConf, req types.AccessRequest) (err error) {
 	requestReason := cf.RequestReason
 	if requestReason == "" {
 		// Prompt for a request reason.
@@ -3282,7 +3301,11 @@ func retryWithAccessRequest(
 		}
 	}
 	req.SetRequestReason(requestReason)
+	return nil
+}
 
+func sendAccessRequestAndWaitForApproval(cf *CLIConf, tc *client.TeleportClient, req types.AccessRequest) (err error) {
+	cf.RequestID = req.GetName()
 	fmt.Fprint(os.Stdout, "Creating request...\n")
 	// Always create access request against the root cluster.
 	if err := tc.WithRootClusterClient(cf.Context, func(clt auth.ClientI) error {
@@ -3313,11 +3336,7 @@ func retryWithAccessRequest(
 	if err := onRequestResolution(cf, tc, resolvedReq); err != nil {
 		return trace.Wrap(err)
 	}
-
-	// Retry now that request has been approved and certs updated.
-	// Clear the original exit status.
-	tc.ExitStatus = 0
-	return trace.Wrap(fn())
+	return nil
 }
 
 func onSSHLatency(cf *CLIConf) error {