diff --git src/wp-admin/css/customize-nav-menus.css src/wp-admin/css/customize-nav-menus.css
index a63df15..6fe558d 100644
--- src/wp-admin/css/customize-nav-menus.css
+++ src/wp-admin/css/customize-nav-menus.css
@@ -301,19 +301,19 @@
 	text-decoration: none !important;
 }
 
-#accordion-panel-nav_menus .field-link-target,
-#accordion-panel-nav_menus .field-title-attribute,
-#accordion-panel-nav_menus .field-css-classes,
-#accordion-panel-nav_menus .field-xfn,
-#accordion-panel-nav_menus .field-description {
+.control-section-nav_menu .field-link-target,
+.control-section-nav_menu .field-title-attribute,
+.control-section-nav_menu .field-css-classes,
+.control-section-nav_menu .field-xfn,
+.control-section-nav_menu .field-description {
 	display: none;
 }
 
-#accordion-panel-nav_menus.field-link-target-active .field-link-target,
-#accordion-panel-nav_menus.field-title-attribute-active .field-title-attribute,
-#accordion-panel-nav_menus.field-css-classes-active .field-css-classes,
-#accordion-panel-nav_menus.field-xfn-active .field-xfn,
-#accordion-panel-nav_menus.field-description-active .field-description {
+.control-section-nav_menu.field-link-target-active .field-link-target,
+.control-section-nav_menu.field-title-attribute-active .field-title-attribute,
+.control-section-nav_menu.field-css-classes-active .field-css-classes,
+.control-section-nav_menu.field-xfn-active .field-xfn,
+.control-section-nav_menu.field-description-active .field-description {
 	display: block;
 }
 
diff --git src/wp-admin/js/customize-nav-menus.js src/wp-admin/js/customize-nav-menus.js
index be3fba1..14c7ef4 100644
--- src/wp-admin/js/customize-nav-menus.js
+++ src/wp-admin/js/customize-nav-menus.js
@@ -786,30 +786,23 @@
 		},
 
 		/**
-		 * Show/hide/save screen options (columns). From common.js.
+		 * Update field visibility when clicking on the field toggles.
 		 */
 		ready: function() {
 			var panel = this;
-			this.container.find( '.hide-column-tog' ).click( function() {
-				var $t = $( this ), column = $t.val();
-				if ( $t.prop( 'checked' ) ) {
-					panel.checked( column );
-				} else {
-					panel.unchecked( column );
-				}
-
+			panel.container.find( '.hide-column-tog' ).click( function() {
 				panel.saveManageColumnsState();
 			});
-			this.container.find( '.hide-column-tog' ).each( function() {
-			var $t = $( this ), column = $t.val();
-				if ( $t.prop( 'checked' ) ) {
-					panel.checked( column );
-				} else {
-					panel.unchecked( column );
-				}
-			});
 		},
 
+		/**
+		 * Save hidden column states.
+		 *
+		 * @since 4.3.0
+		 * @private
+		 *
+		 * @returns {void}
+		 */
 		saveManageColumnsState: _.debounce( function() {
 			var panel = this;
 			if ( panel._updateHiddenColumnsRequest ) {
@@ -826,14 +819,24 @@
 			} );
 		}, 2000 ),
 
-		checked: function( column ) {
-			this.container.addClass( 'field-' + column + '-active' );
-		},
+		/**
+		 * @deprecated Since 4.7.0 now that the nav_menu sections are responsible for toggling the classes on their own containers.
+		 */
+		checked: function() {},
 
-		unchecked: function( column ) {
-			this.container.removeClass( 'field-' + column + '-active' );
-		},
+		/**
+		 * @deprecated Since 4.7.0 now that the nav_menu sections are responsible for toggling the classes on their own containers.
+		 */
+		unchecked: function() {},
 
+		/**
+		 * Get hidden fields.
+		 *
+		 * @since 4.3.0
+		 * @private
+		 *
+		 * @returns {Array} Fields (columns) that are hidden.
+		 */
 		hidden: function() {
 			return $( '.hide-column-tog' ).not( ':checked' ).map( function() {
 				var id = this.id;
@@ -871,7 +874,7 @@
 		 * Ready.
 		 */
 		ready: function() {
-			var section = this;
+			var section = this, fieldActiveToggles, handleFieldActiveToggle;
 
 			if ( 'undefined' === typeof section.params.menu_id ) {
 				throw new Error( 'params.menu_id was not defined' );
@@ -923,6 +926,20 @@
 				section.container.find( '.menu-item.move-left-disabled .menus-move-left' ).attr({ 'tabindex': '-1', 'aria-hidden': 'true' });
 				section.container.find( '.menu-item.move-right-disabled .menus-move-right' ).attr({ 'tabindex': '-1', 'aria-hidden': 'true' });
 			} );
+
+			/**
+			 * Update the active field class for the content container for a given checkbox toggle.
+			 *
+			 * @this {jQuery}
+			 * @returns {void}
+			 */
+			handleFieldActiveToggle = function() {
+				var className = 'field-' + $( this ).val() + '-active';
+				section.contentContainer.toggleClass( className, $( this ).prop( 'checked' ) );
+			};
+			fieldActiveToggles = api.panel( 'nav_menus' ).contentContainer.find( '.metabox-prefs:first' ).find( '.hide-column-tog' );
+			fieldActiveToggles.each( handleFieldActiveToggle );
+			fieldActiveToggles.on( 'click', handleFieldActiveToggle );
 		},
 
 		populateControls: function() {