diff --git a/daemon/libnetwork/sandbox_dns_unix.go b/daemon/libnetwork/sandbox_dns_unix.go
index ca18a75919..a28181b896 100644
--- a/daemon/libnetwork/sandbox_dns_unix.go
+++ b/daemon/libnetwork/sandbox_dns_unix.go
@@ -264,8 +264,17 @@ func (sb *Sandbox) loadResolvConf(path string) (*resolvconf.ResolvConf, error) {
 // be a copy of the host's file, with overrides for nameservers, options and search
 // domains applied.
 func (sb *Sandbox) setupDNS() error {
-	// Make sure the directory exists.
 	sb.restoreResolvConfPath()
+
+	// When the container is restarted, a new Sandbox is created but the same resolv.conf is re-used. If it was
+	// user-modified, do not attempt to overwrite it.
+	if !sb.config.useDefaultSandBox {
+		if mod, err := resolvconf.UserModified(sb.config.resolvConfPath, sb.config.resolvConfHashFile); err != nil || mod {
+			return err
+		}
+	}
+
+	// Make sure the directory exists.
 	dir, _ := filepath.Split(sb.config.resolvConfPath)
 	if err := createBasePath(dir); err != nil {
 		return err
diff --git a/daemon/libnetwork/sandbox_dns_unix_test.go b/daemon/libnetwork/sandbox_dns_unix_test.go
index 3bb64cf5ce..49439d3571 100644
--- a/daemon/libnetwork/sandbox_dns_unix_test.go
+++ b/daemon/libnetwork/sandbox_dns_unix_test.go
@@ -14,12 +14,17 @@ import (
 	is "gotest.tools/v3/assert/cmp"
 )
 
-func getResolvConfOptions(t *testing.T, rcPath string) []string {
+func getResolvConf(t *testing.T, rcPath string) resolvconf.ResolvConf {
 	t.Helper()
 	resolv, err := os.ReadFile(rcPath)
 	assert.NilError(t, err)
 	rc, err := resolvconf.Parse(bytes.NewBuffer(resolv), "")
 	assert.NilError(t, err)
+	return rc
+}
+
+func getResolvConfOptions(t *testing.T, rcPath string) []string {
+	rc := getResolvConf(t, rcPath)
 	return rc.Options()
 }
 
@@ -90,3 +95,60 @@ func TestDNSOptions(t *testing.T) {
 	dnsOptionsList = getResolvConfOptions(t, sb2.config.resolvConfPath)
 	assert.Check(t, is.DeepEqual([]string{"ndots:0"}, dnsOptionsList))
 }
+
+func TestNonHostNetDNSRestart(t *testing.T) {
+	c, err := New(context.Background(), config.OptionDataDir(t.TempDir()))
+	assert.NilError(t, err)
+
+	// Step 1: Create initial sandbox (simulating first container start)
+	sb, err := c.NewSandbox(context.Background(), "cnt1")
+	assert.NilError(t, err)
+
+	defer func() {
+		_ = sb.Delete(context.Background())
+	}()
+
+	sb.startResolver(false)
+
+	err = sb.setupDNS()
+	assert.NilError(t, err)
+	err = sb.rebuildDNS()
+	assert.NilError(t, err)
+
+	// Step 2: Simulate user manually overwriting the container's resolv.conf
+	resolvConfPath := sb.config.resolvConfPath
+	modifiedContent := []byte(`nameserver 1.1.1.1`)
+	err = os.WriteFile(resolvConfPath, modifiedContent, 0644)
+	assert.NilError(t, err)
+
+	// Step 3: Delete the sandbox (simulating container stop)
+	err = sb.Delete(context.Background())
+	assert.NilError(t, err)
+
+	// Step 4: Create a new sandbox (simulating container restart)
+	sbRestart, err := c.NewSandbox(context.Background(), "cnt1",
+		OptionResolvConfPath(resolvConfPath),
+	)
+	assert.NilError(t, err)
+	defer func() {
+		if err := sbRestart.Delete(context.Background()); err != nil {
+			t.Error(err)
+		}
+	}()
+
+	sbRestart.startResolver(false)
+
+	// Step 5: Call setupDNS on restart - should preserve user modifications
+	err = sbRestart.setupDNS()
+	assert.NilError(t, err)
+
+	rc := getResolvConf(t, sbRestart.config.resolvConfPath)
+	assert.Check(t, is.Equal("1.1.1.1", rc.NameServers()[0].String()))
+
+	// Step 6: Call rebuildDNS on restart - should preserve user modifications
+	err = sbRestart.rebuildDNS()
+	assert.NilError(t, err)
+
+	rc = getResolvConf(t, sbRestart.config.resolvConfPath)
+	assert.Check(t, is.Equal("1.1.1.1", rc.NameServers()[0].String()))
+}
diff --git a/integration/networking/resolvconf_test.go b/integration/networking/resolvconf_test.go
index c0119bd650..7f5caa3a8f 100644
--- a/integration/networking/resolvconf_test.go
+++ b/integration/networking/resolvconf_test.go
@@ -212,3 +212,41 @@ func TestNslookupWindows(t *testing.T) {
 	// can only be changed in daemon.json using feature flag "windows-dns-proxy".
 	assert.Check(t, is.Contains(res.Stdout.String(), "Addresses:"))
 }
+
+// TestResolvConfPreservedOnRestart verifies that external modifications to
+// /etc/resolv.conf are preserved when a non-host network container is restarted.
+// Regression test for https://github.com/moby/moby/issues/51490
+func TestResolvConfPreservedOnRestart(t *testing.T) {
+	skip.If(t, testEnv.DaemonInfo.OSType == "windows", "No /etc/resolv.conf on Windows")
+
+	ctx := setupTest(t)
+
+	d := daemon.New(t, daemon.WithResolvConf(network.GenResolvConf("8.8.8.8")))
+	d.StartWithBusybox(ctx, t)
+	defer d.Stop(t)
+
+	c := d.NewClientT(t)
+	defer c.Close()
+
+	const ctrName = "test-resolvconf-preserved-on-restart"
+	id := container.Run(ctx, t, c, container.WithName(ctrName))
+	defer c.ContainerRemove(ctx, id, client.ContainerRemoveOptions{Force: true})
+
+	appendContent := `# hello`
+	res, err := container.Exec(ctx, c, ctrName, []string{
+		"sh", "-c",
+		"echo '" + appendContent + "' >> /etc/resolv.conf",
+	})
+	assert.NilError(t, err)
+	assert.Check(t, is.Equal(res.ExitCode, 0))
+
+	// Restart the container.
+	_, err = c.ContainerRestart(ctx, ctrName, client.ContainerRestartOptions{})
+	assert.Assert(t, is.Nil(err))
+
+	// Verify the modification was preserved
+	res, err = container.Exec(ctx, c, ctrName, []string{"tail", "-n", "1", "/etc/resolv.conf"})
+	assert.NilError(t, err)
+	assert.Check(t, is.Equal(res.ExitCode, 0))
+	assert.Check(t, is.Contains(res.Stdout(), appendContent))
+}