diff --git a/daemon/libnetwork/sandbox.go b/daemon/libnetwork/sandbox.go
index 4d0236f2e4..8f5e531188 100644
--- a/daemon/libnetwork/sandbox.go
+++ b/daemon/libnetwork/sandbox.go
@@ -348,10 +348,8 @@ func (sb *Sandbox) populateNetworkResources(ctx context.Context, ep *Endpoint) (
 
 	// Populate DNS records.
 	n := ep.getNetwork()
-	if !n.getController().isAgent() {
-		if !n.getController().isSwarmNode() || n.Scope() != scope.Swarm || !n.driverIsMultihost() {
-			n.updateSvcRecord(context.WithoutCancel(ctx), ep, true)
-		}
+	if !n.getController().isSwarmNode() || n.Scope() != scope.Swarm || !n.driverIsMultihost() {
+		n.updateSvcRecord(context.WithoutCancel(ctx), ep, true)
 	}
 
 	if err := ep.addDriverInfoToCluster(); err != nil {
diff --git a/integration/networking/bridge_linux_test.go b/integration/networking/bridge_linux_test.go
index 4fd27e74f2..705da61d4b 100644
--- a/integration/networking/bridge_linux_test.go
+++ b/integration/networking/bridge_linux_test.go
@@ -1092,7 +1092,7 @@ func TestDisableIPv6OnInterface(t *testing.T) {
 			// There should not be an IPv6 DNS or /etc/hosts entry.
 			runRes := container.RunAttach(ctx, t, c,
 				container.WithNetworkMode(tc.netName),
-				container.WithCmd("ping", "-6", ctrName),
+				container.WithCmd("ping", "-6", "-c1", ctrName),
 			)
 			assert.Check(t, is.Equal(runRes.ExitCode, 1))
 			assert.Check(t, is.Contains(runRes.Stderr.String(), "bad address"))
@@ -2032,3 +2032,29 @@ func TestLegacyLinksEnvVars(t *testing.T) {
 		})
 	}
 }
+
+// TestDNSNamesForNonSwarmScopedNetworks checks that container names can be resolved for non-swarm-scoped networks once
+// a node has joined a Swarm cluster.
+//
+// Regression test for https://github.com/moby/moby/issues/51491.
+func TestDNSNamesForNonSwarmScopedNetworks(t *testing.T) {
+	ctx := setupTest(t)
+
+	d := daemon.New(t)
+	d.StartAndSwarmInit(ctx, t)
+	defer d.Stop(t)
+
+	c := d.NewClientT(t)
+	defer c.Close()
+
+	const bridgeName = "dnsnames-with-swarm"
+	network.CreateNoError(ctx, t, c, bridgeName)
+	defer network.RemoveNoError(ctx, t, c, bridgeName)
+
+	res := container.RunAttach(ctx, t, c,
+		container.WithName("test"),
+		container.WithCmd("nslookup", "-type=a", "test."),
+		container.WithNetworkMode(bridgeName),
+		container.WithAutoRemove)
+	assert.Equal(t, res.ExitCode, 0, "exit code: %d, expected 0; stdout:\n%s", res.ExitCode, res.Stdout)
+}