diff --git a/staging/src/k8s.io/apiserver/pkg/storage/cacher/cacher.go b/staging/src/k8s.io/apiserver/pkg/storage/cacher/cacher.go
index aee122521af..4453b5cf1d3 100644
--- a/staging/src/k8s.io/apiserver/pkg/storage/cacher/cacher.go
+++ b/staging/src/k8s.io/apiserver/pkg/storage/cacher/cacher.go
@@ -922,12 +922,24 @@ func (c *Cacher) dispatchEvents() {
 			bookmarkTimer.Reset(wait.Jitter(time.Second, 0.25))
 			// Never send a bookmark event if we did not see an event here, this is fine
 			// because we don't provide any guarantees on sending bookmarks.
+			//
+			// Just pop closed watchers and requeue others if needed.
+			//
+			// TODO(#115478): rework the following logic
+			//  in a way that would allow more
+			//  efficient cleanup of closed watchers
 			if lastProcessedResourceVersion == 0 {
 				func() {
 					c.Lock()
 					defer c.Unlock()
-					// pop expired watchers in case there has been no update
-					c.bookmarkWatchers.popExpiredWatchersThreadUnsafe()
+					for _, watchers := range c.bookmarkWatchers.popExpiredWatchersThreadUnsafe() {
+						for _, watcher := range watchers {
+							if watcher.stopped {
+								continue
+							}
+							c.bookmarkWatchers.addWatcherThreadUnsafe(watcher)
+						}
+					}
 				}()
 				continue
 			}
diff --git a/staging/src/k8s.io/apiserver/pkg/storage/cacher/cacher_whitebox_test.go b/staging/src/k8s.io/apiserver/pkg/storage/cacher/cacher_whitebox_test.go
index 24e0da48b25..86d184e136c 100644
--- a/staging/src/k8s.io/apiserver/pkg/storage/cacher/cacher_whitebox_test.go
+++ b/staging/src/k8s.io/apiserver/pkg/storage/cacher/cacher_whitebox_test.go
@@ -1973,3 +1973,59 @@ func BenchmarkCacher_GetList(b *testing.B) {
 			})
 	}
 }
+
+// TestDoNotPopExpiredWatchersWhenNoEventsSeen makes sure that
+// a bookmark event will be delivered after the cacher has seen an event.
+// Previously the watchers have been removed from the "want bookmark" queue.
+func TestDoNotPopExpiredWatchersWhenNoEventsSeen(t *testing.T) {
+	defer featuregatetesting.SetFeatureGateDuringTest(t, utilfeature.DefaultFeatureGate, features.WatchList, true)()
+	backingStorage := &dummyStorage{}
+	cacher, _, err := newTestCacher(backingStorage)
+	if err != nil {
+		t.Fatalf("Couldn't create cacher: %v", err)
+	}
+	defer cacher.Stop()
+
+	// wait until cacher is initialized.
+	if err := cacher.ready.wait(context.Background()); err != nil {
+		t.Fatalf("unexpected error waiting for the cache to be ready")
+	}
+
+	pred := storage.Everything
+	pred.AllowWatchBookmarks = true
+	opts := storage.ListOptions{
+		Predicate:         pred,
+		SendInitialEvents: pointer.Bool(true),
+	}
+	w, err := cacher.Watch(context.Background(), "pods/ns", opts)
+	require.NoError(t, err, "failed to create watch: %v")
+	defer w.Stop()
+
+	// Ensure that popExpiredWatchers is called to ensure that our watch isn't removed from bookmarkWatchers.
+	// We do that every ~1s, so waiting 2 seconds seems enough.
+	time.Sleep(2 * time.Second)
+
+	// Send an event to ensure that lastProcessedResourceVersion in Cacher will change to non-zero value.
+	makePod := func(rv uint64) *example.Pod {
+		return &example.Pod{
+			ObjectMeta: metav1.ObjectMeta{
+				Name:            fmt.Sprintf("pod-%d", rv),
+				Namespace:       "ns",
+				ResourceVersion: fmt.Sprintf("%d", rv),
+				Annotations:     map[string]string{},
+			},
+		}
+	}
+	err = cacher.watchCache.Add(makePod(102))
+	require.NoError(t, err)
+
+	verifyEvents(t, w, []watch.Event{
+		{Type: watch.Added, Object: makePod(102)},
+		{Type: watch.Bookmark, Object: &example.Pod{
+			ObjectMeta: metav1.ObjectMeta{
+				ResourceVersion: "102",
+				Annotations:     map[string]string{"k8s.io/initial-events-end": "true"},
+			},
+		}},
+	}, true)
+}