diff --git a/staging/src/k8s.io/apiserver/pkg/server/genericapiserver.go b/staging/src/k8s.io/apiserver/pkg/server/genericapiserver.go
index 2377fb8fec0..fec8da9faa6 100644
--- a/staging/src/k8s.io/apiserver/pkg/server/genericapiserver.go
+++ b/staging/src/k8s.io/apiserver/pkg/server/genericapiserver.go
@@ -191,7 +191,7 @@ type GenericAPIServer struct {
 	livezGracePeriod      time.Duration
 	livezClock            clock.Clock
 
-	// auditing. The backend is started after the server starts listening.
+	// auditing. The backend is started before the server starts listening.
 	AuditBackend audit.Backend
 
 	// Authorizer determines whether a user is allowed to make a certain request. The Handler does a preliminary
@@ -512,10 +512,20 @@ func (s preparedGenericAPIServer) Run(stopCh <-chan struct{}) error {
 		<-preShutdownHooksHasStoppedCh
 	}()
 
+	// Start the audit backend before any request comes in. This means we must call Backend.Run
+	// before http server start serving. Otherwise the Backend.ProcessEvents call might block.
+	// AuditBackend.Run will stop as soon as all in-flight requests are drained.
+	if s.AuditBackend != nil {
+		if err := s.AuditBackend.Run(drainedCh.Signaled()); err != nil {
+			return fmt.Errorf("failed to run the audit backend: %v", err)
+		}
+	}
+
 	stoppedCh, listenerStoppedCh, err := s.NonBlockingRun(stopHttpServerCh, shutdownTimeout)
 	if err != nil {
 		return err
 	}
+
 	httpServerStoppedListeningCh := s.lifecycleSignals.HTTPServerStoppedListening
 	go func() {
 		<-listenerStoppedCh
@@ -561,18 +571,6 @@ func (s preparedGenericAPIServer) Run(stopCh <-chan struct{}) error {
 // returned if the secure port cannot be listened on.
 // The returned channel is closed when the (asynchronous) termination is finished.
 func (s preparedGenericAPIServer) NonBlockingRun(stopCh <-chan struct{}, shutdownTimeout time.Duration) (<-chan struct{}, <-chan struct{}, error) {
-	// Use an stop channel to allow graceful shutdown without dropping audit events
-	// after http server shutdown.
-	auditStopCh := make(chan struct{})
-
-	// Start the audit backend before any request comes in. This means we must call Backend.Run
-	// before http server start serving. Otherwise the Backend.ProcessEvents call might block.
-	if s.AuditBackend != nil {
-		if err := s.AuditBackend.Run(auditStopCh); err != nil {
-			return nil, nil, fmt.Errorf("failed to run the audit backend: %v", err)
-		}
-	}
-
 	// Use an internal stop channel to allow cleanup of the listeners on error.
 	internalStopCh := make(chan struct{})
 	var stoppedCh <-chan struct{}
@@ -582,7 +580,6 @@ func (s preparedGenericAPIServer) NonBlockingRun(stopCh <-chan struct{}, shutdow
 		stoppedCh, listenerStoppedCh, err = s.SecureServingInfo.Serve(s.Handler, shutdownTimeout, internalStopCh)
 		if err != nil {
 			close(internalStopCh)
-			close(auditStopCh)
 			return nil, nil, err
 		}
 	}
@@ -597,7 +594,6 @@ func (s preparedGenericAPIServer) NonBlockingRun(stopCh <-chan struct{}, shutdow
 			<-stoppedCh
 		}
 		s.HandlerChainWaitGroup.Wait()
-		close(auditStopCh)
 	}()
 
 	s.RunPostStartHooks(stopCh)