diff --git a/pkg/agent/controller/endpoint_slice.go b/pkg/agent/controller/endpoint_slice.go
index 3e2524096..3eb805181 100644
--- a/pkg/agent/controller/endpoint_slice.go
+++ b/pkg/agent/controller/endpoint_slice.go
@@ -23,6 +23,7 @@ import (
 	"fmt"
 	"strconv"
 	"strings"
+	"time"
 
 	"github.com/pkg/errors"
 	"github.com/submariner-io/admiral/pkg/log"
@@ -36,6 +37,7 @@ import (
 	metav1 "k8s.io/apimachinery/pkg/apis/meta/v1"
 	k8slabels "k8s.io/apimachinery/pkg/labels"
 	"k8s.io/apimachinery/pkg/runtime"
+	"k8s.io/apimachinery/pkg/util/wait"
 	mcsv1a1 "sigs.k8s.io/mcs-api/pkg/apis/v1alpha1"
 )
 
@@ -62,8 +64,8 @@ func newEndpointSliceController(spec *AgentSpecification, syncerConfig broker.Sy
 			OnSuccessfulSyncToBroker: c.onLocalEndpointSliceSynced,
 			BrokerResourceType:       &discovery.EndpointSlice{},
 			TransformBrokerToLocal:   c.onRemoteEndpointSlice,
-			OnSuccessfulSyncFromBroker: func(obj runtime.Object, _ syncer.Operation) bool {
-				c.enqueueForConflictCheck(obj.(*discovery.EndpointSlice))
+			OnSuccessfulSyncFromBroker: func(obj runtime.Object, op syncer.Operation) bool {
+				c.enqueueForConflictCheck(obj.(*discovery.EndpointSlice), op)
 				return false
 			},
 			BrokerResyncPeriod: BrokerResyncePeriod,
@@ -162,7 +164,7 @@ func (c *EndpointSliceController) onLocalEndpointSliceSynced(obj runtime.Object,
 			c.serviceExportClient.updateStatusConditions(serviceName, serviceNamespace, newServiceExportCondition(constants.ServiceExportReady,
 				corev1.ConditionTrue, "", "Service was successfully exported to the broker"))
 
-			c.enqueueForConflictCheck(endpointSlice)
+			c.enqueueForConflictCheck(endpointSlice, op)
 		}
 	}
 
@@ -198,29 +200,21 @@ func (c *EndpointSliceController) hasNoRemainingEndpointSlices(endpointSlice *di
 	return true
 }
 
-func (c *EndpointSliceController) checkForConflicts(key, name, namespace string) (bool, error) {
+func (c *EndpointSliceController) checkForConflicts(_, name, namespace string) (bool, error) {
 	localServiceExport := c.serviceExportClient.getLocalInstance(name, namespace)
 	if localServiceExport == nil {
 		return false, nil
 	}
 
-	epsList, err := c.syncer.GetLocalClient().Resource(endpointSliceGVR).Namespace(namespace).List(context.Background(), metav1.ListOptions{
-		LabelSelector: k8slabels.SelectorFromSet(map[string]string{
-			discovery.LabelManagedBy: constants.LabelValueManagedBy,
-			mcsv1a1.LabelServiceName: name,
-		}).String(),
-	})
-	if err != nil {
-		return true, errors.Wrapf(err, "error during conflict check for %q", key)
-	}
+	epsList := c.syncer.ListLocalResources(&discovery.EndpointSlice{})
 
 	var prevServicePorts []mcsv1a1.ServicePort
 	var intersectedServicePorts []mcsv1a1.ServicePort
-	clusterNames := make([]string, 0, len(epsList.Items))
+	clusterNames := make([]string, 0, len(epsList))
 	conflict := false
 
-	for i := range epsList.Items {
-		eps := c.serviceExportClient.toEndpointSlice(&epsList.Items[i])
+	for _, o := range epsList {
+		eps := o.(*discovery.EndpointSlice)
 
 		servicePorts := c.serviceExportClient.toServicePorts(eps.Ports)
 		if prevServicePorts == nil {
@@ -248,11 +242,20 @@ func (c *EndpointSliceController) checkForConflicts(key, name, namespace string)
 	return false, nil
 }
 
-func (c *EndpointSliceController) enqueueForConflictCheck(eps *discovery.EndpointSlice) {
+func (c *EndpointSliceController) enqueueForConflictCheck(eps *discovery.EndpointSlice, op syncer.Operation) {
 	if eps.Labels[constants.LabelIsHeadless] != "false" {
 		return
 	}
 
+	// Since the conflict checking works off of the local cache for efficiency, wait a little bit here for the local cache to be updated
+	// with the latest state of the EndpointSlice.
+	_ = wait.PollUntilContextTimeout(context.Background(), 10*time.Millisecond, 100*time.Millisecond, true,
+		func(_ context.Context) (bool, error) {
+			_, found, _ := c.syncer.GetLocalResource(eps.Name, eps.Namespace, eps)
+			return (op == syncer.Delete && !found) || (op != syncer.Delete && found), nil
+		},
+	)
+
 	c.conflictCheckWorkQueue.Enqueue(&discovery.EndpointSlice{
 		ObjectMeta: metav1.ObjectMeta{
 			Name:      eps.Labels[mcsv1a1.LabelServiceName],