diff --git src/wp-includes/class-wp-customize-nav-menus.php src/wp-includes/class-wp-customize-nav-menus.php
index 3d9e60f..40a7f6b 100644
--- src/wp-includes/class-wp-customize-nav-menus.php
+++ src/wp-includes/class-wp-customize-nav-menus.php
@@ -795,10 +795,11 @@ final class WP_Customize_Nav_Menus {
 	 */
 	public function filter_wp_nav_menu( $nav_menu_content, $args ) {
 		if ( ! empty( $args->can_partial_refresh ) && ! empty( $args->instance_number ) ) {
-			$nav_menu_content = sprintf(
-				'<div id="partial-refresh-menu-container-%1$d" class="partial-refresh-menu-container" data-instance-number="%1$d">%2$s</div>',
-				$args->instance_number,
-				$nav_menu_content
+			$nav_menu_content = preg_replace(
+				'/(?<=class=")/',
+				sprintf( 'partial-refreshable-nav-menu partial-refreshable-nav-menu-%1$d ', $args->instance_number ),
+				$nav_menu_content,
+				1 // Only update the class on the first element found, the menu container.
 			);
 		}
 		return $nav_menu_content;
diff --git src/wp-includes/js/customize-preview-nav-menus.js src/wp-includes/js/customize-preview-nav-menus.js
index 2b6c994..4b9ac08 100644
--- src/wp-includes/js/customize-preview-nav-menus.js
+++ src/wp-includes/js/customize-preview-nav-menus.js
@@ -163,14 +163,15 @@ wp.customize.menusPreview = ( function( $, api ) {
 	 * @param {int} instanceNumber
 	 */
 	self.refreshMenuInstance = function( instanceNumber ) {
-		var self = this, data, customized, container, request, wpNavArgs, instance;
+		var self = this, data, customized, container, request, wpNavArgs, instance, containerInstanceClassName;
 
 		if ( ! self.navMenuInstanceArgs[ instanceNumber ] ) {
 			throw new Error( 'unknown_instance_number' );
 		}
 		instance = self.navMenuInstanceArgs[ instanceNumber ];
 
-		container = $( '#partial-refresh-menu-container-' + String( instanceNumber ) );
+		containerInstanceClassName = 'partial-refreshable-nav-menu-' + String( instanceNumber );
+		container = $( '.' + containerInstanceClassName );
 
 		if ( ! instance.can_partial_refresh || 0 === container.length ) {
 			api.preview.send( 'refresh' );
@@ -207,19 +208,23 @@ wp.customize.menusPreview = ( function( $, api ) {
 			url: self.requestUri
 		} );
 		request.done( function( data ) {
-			var eventParam;
-			container.empty().append( $( data ) );
+			// If the menu is now not visible, refresh since the page layout may have changed.
+			if ( false === data ) {
+				api.preview.send( 'refresh' );
+				return;
+			}
+
+			var eventParam, previousContainer = container;
+			container = $( data );
+			container.addClass( containerInstanceClassName );
+			container.addClass( 'partial-refreshable-nav-menu customize-partial-refreshing' );
+			previousContainer.replaceWith( container );
 			eventParam = {
 				instanceNumber: instanceNumber,
 				wpNavArgs: wpNavArgs
 			};
-			$( document ).trigger( 'customize-preview-menu-refreshed', [ eventParam ] );
-		} );
-		request.fail( function() {
-			// @todo provide some indication for why
-		} );
-		request.always( function() {
 			container.removeClass( 'customize-partial-refreshing' );
+			$( document ).trigger( 'customize-preview-menu-refreshed', [ eventParam ] );
 		} );
 	};