diff --git a/lib/services/access_request_cache.go b/lib/services/access_request_cache.go
index 100458ef49061..ff23fe2d278ad 100644
--- a/lib/services/access_request_cache.go
+++ b/lib/services/access_request_cache.go
@@ -53,6 +53,8 @@ type AccessRequestCacheConfig struct {
 	Events types.Events
 	// Getter is an access request getter client.
 	Getter AccessRequestGetter
+	// MaxRetryPeriod is the maximum retry period on failed watches.
+	MaxRetryPeriod time.Duration
 }
 
 // CheckAndSetDefaults valides the config and provides reasonable defaults for optional fields.
@@ -84,8 +86,12 @@ type AccessRequestCache struct {
 	primaryCache *sortcache.SortCache[*types.AccessRequestV3]
 	ttlCache     *utils.FnCache
 	initC        chan struct{}
+	initOnce     sync.Once
 	closeContext context.Context
 	cancel       context.CancelFunc
+	// onInit is a callback used in tests to detect
+	// individual initializations.
+	onInit func()
 }
 
 // NewAccessRequestCache sets up a new [AccessRequestCache] instance based on the supplied
@@ -117,8 +123,9 @@ func NewAccessRequestCache(cfg AccessRequestCacheConfig) (*AccessRequestCache, e
 	}
 
 	if _, err := newResourceWatcher(ctx, c, ResourceWatcherConfig{
-		Component: "access-request-cache",
-		Client:    cfg.Events,
+		Component:      "access-request-cache",
+		Client:         cfg.Events,
+		MaxRetryPeriod: cfg.MaxRetryPeriod,
 	}); err != nil {
 		cancel()
 		return nil, trace.Wrap(err)
@@ -344,11 +351,23 @@ func (c *AccessRequestCache) getResourcesAndUpdateCurrent(ctx context.Context) e
 	c.rw.Lock()
 	defer c.rw.Unlock()
 	c.primaryCache = cache
-	close(c.initC)
+	c.initOnce.Do(func() {
+		close(c.initC)
+	})
+	if c.onInit != nil {
+		c.onInit()
+	}
 	return nil
 }
 
-// processEventAndUpdateCurrent is part of the resourceCollector interface and is used to update the
+// SetInitCallback is used in tests that care about cache inits.
+func (c *AccessRequestCache) SetInitCallback(cb func()) {
+	c.rw.Lock()
+	defer c.rw.Unlock()
+	c.onInit = cb
+}
+
+// processEventsAndUpdateCurrent is part of the resourceCollector interface and is used to update the
 // primary cache state when modification events occur.
 func (c *AccessRequestCache) processEventAndUpdateCurrent(ctx context.Context, event types.Event) {
 	c.rw.RLock()
@@ -385,6 +404,7 @@ func (c *AccessRequestCache) notifyStale() {
 	}
 	c.primaryCache = nil
 	c.initC = make(chan struct{})
+	c.initOnce = sync.Once{}
 }
 
 // initializationChan is part of the resourceCollector interface and gets the channel
diff --git a/lib/services/access_request_cache_test.go b/lib/services/access_request_cache_test.go
index d34aa948fe064..decd85684fe71 100644
--- a/lib/services/access_request_cache_test.go
+++ b/lib/services/access_request_cache_test.go
@@ -22,7 +22,10 @@ import (
 	"testing"
 	"time"
 
+	"github.com/google/uuid"
+	"github.com/gravitational/trace"
 	"github.com/stretchr/testify/require"
+	"golang.org/x/sync/errgroup"
 
 	"github.com/gravitational/teleport/api/client/proto"
 	"github.com/gravitational/teleport/api/types"
@@ -34,6 +37,8 @@ import (
 type accessRequestServices struct {
 	types.Events
 	services.DynamicAccessExt
+
+	bk *memory.Memory
 }
 
 func newAccessRequestPack(t *testing.T) (accessRequestServices, *services.AccessRequestCache) {
@@ -43,11 +48,13 @@ func newAccessRequestPack(t *testing.T) (accessRequestServices, *services.Access
 	svcs := accessRequestServices{
 		Events:           local.NewEventsService(bk),
 		DynamicAccessExt: local.NewDynamicAccessService(bk),
+		bk:               bk,
 	}
 
 	cache, err := services.NewAccessRequestCache(services.AccessRequestCacheConfig{
-		Events: svcs,
-		Getter: svcs,
+		Events:         svcs,
+		Getter:         svcs,
+		MaxRetryPeriod: time.Millisecond * 100,
 	})
 	require.NoError(t, err)
 
@@ -60,6 +67,108 @@ func newAccessRequestPack(t *testing.T) (accessRequestServices, *services.Access
 	return svcs, cache
 }
 
+func TestAccessRequestCacheResets(t *testing.T) {
+	const (
+		requestCount = 100
+		workers      = 20
+		resets       = 3
+	)
+
+	t.Parallel()
+
+	svcs, cache := newAccessRequestPack(t)
+	defer cache.Close()
+
+	ctx, cancel := context.WithCancel(context.Background())
+	defer cancel()
+
+	for i := 0; i < requestCount; i++ {
+		r, err := types.NewAccessRequest(uuid.New().String(), "alice@example.com", "some-role")
+		require.NoError(t, err)
+
+		_, err = svcs.CreateAccessRequestV2(ctx, r)
+		require.NoError(t, err)
+	}
+
+	timeout := time.After(time.Second * 30)
+
+	for {
+		rsp, err := cache.ListAccessRequests(ctx, &proto.ListAccessRequestsRequest{
+			Limit: requestCount,
+		})
+		require.NoError(t, err)
+		if len(rsp.AccessRequests) == requestCount {
+			break
+		}
+
+		select {
+		case <-timeout:
+			require.FailNow(t, "timeout waiting for access request cache to populate")
+		case <-time.After(time.Millisecond * 200):
+		}
+	}
+
+	doneC := make(chan struct{})
+	reads := make(chan struct{}, workers)
+	var eg errgroup.Group
+
+	for i := 0; i < workers; i++ {
+		eg.Go(func() error {
+			for {
+				select {
+				case <-doneC:
+					return nil
+				case <-time.After(time.Millisecond * 20):
+				}
+
+				rsp, err := cache.ListAccessRequests(ctx, &proto.ListAccessRequestsRequest{
+					Limit: int32(requestCount),
+				})
+				if err != nil {
+					return trace.Errorf("unexpected read failure: %v", err)
+				}
+
+				select {
+				case reads <- struct{}{}:
+				default:
+				}
+
+				if len(rsp.AccessRequests) != requestCount {
+					return trace.Errorf("unexpected number of access requests: %d (expected %d)", len(rsp.AccessRequests), requestCount)
+				}
+			}
+		})
+	}
+
+	inits := make(chan struct{}, resets+1)
+	cache.SetInitCallback(func() {
+		inits <- struct{}{}
+	})
+
+	timeout = time.After(time.Second * 30)
+	for i := 0; i < resets; i++ {
+		svcs.bk.CloseWatchers()
+		select {
+		case <-inits:
+		case <-timeout:
+			require.FailNowf(t, "timeout waiting for access request cache to reset", "reset=%d", i)
+		}
+
+		for j := 0; j < workers; j++ {
+			// ensure that we're not racing ahead of worker reads too
+			// much if inits are happening quickly.
+			select {
+			case <-reads:
+			case <-timeout:
+				require.FailNowf(t, "timeout waiting for worker reads to catch up", "reset=%d", i)
+			}
+		}
+	}
+
+	close(doneC)
+	require.NoError(t, eg.Wait())
+}
+
 // TestAccessRequestCacheBasics verifies the basic expected behaviors of the access request cache,
 // including correct sorting and handling of put/delete events.
 func TestAccessRequestCacheBasics(t *testing.T) {