diff --git a/src/wp-admin/js/customize-controls.js b/src/wp-admin/js/customize-controls.js
index e35ec4fdd8..4f04de4c0f 100644
--- a/src/wp-admin/js/customize-controls.js
+++ b/src/wp-admin/js/customize-controls.js
@@ -2358,11 +2358,23 @@
 
 			messenger.targetWindow( iframe[0].contentWindow );
 
-			messenger.bind( 'login', function() {
-				iframe.remove();
-				messenger.destroy();
-				delete previewer._login;
-				deferred.resolve();
+			messenger.bind( 'login', function () {
+				var refreshNonces = previewer.refreshNonces();
+
+				refreshNonces.always( function() {
+					iframe.remove();
+					messenger.destroy();
+					delete previewer._login;
+				});
+
+				refreshNonces.done( function() {
+					deferred.resolve();
+				});
+
+				refreshNonces.fail( function() {
+					previewer.cheatin();
+					deferred.reject();
+				});
 			});
 
 			return this._login;
@@ -2370,6 +2382,28 @@
 
 		cheatin: function() {
 			$( document.body ).empty().addClass('cheatin').append( '<p>' + api.l10n.cheatin + '</p>' );
+		},
+
+		refreshNonces: function() {
+			var request, deferred = $.Deferred();
+
+			deferred.promise();
+
+			request = wp.ajax.post( 'customize_refresh_nonces', {
+				wp_customize: 'on',
+				theme: api.settings.theme.stylesheet
+			});
+
+			request.done( function( response ) {
+				api.trigger( 'nonce-refresh', response );
+				deferred.resolve();
+			});
+
+			request.fail( function() {
+				deferred.reject();
+			});
+
+			return deferred;
 		}
 	});
 
@@ -2538,6 +2572,12 @@
 			$.extend( this.nonce, nonce );
 		});
 
+		// Refresh the nonces if login sends updated nonces over.
+		api.bind( 'nonce-refresh', function( nonce ) {
+			$.extend( api.settings.nonce, nonce );
+			$.extend( api.previewer.nonce, nonce );
+		});
+
 		// Create Settings
 		$.each( api.settings.settings, function( id, data ) {
 			api.create( id, id, data.value, {
diff --git a/src/wp-admin/js/customize-widgets.js b/src/wp-admin/js/customize-widgets.js
index 8134a984d3..20c695b621 100644
--- a/src/wp-admin/js/customize-widgets.js
+++ b/src/wp-admin/js/customize-widgets.js
@@ -1898,6 +1898,11 @@
 		sidebar_widgets: api.Widgets.SidebarControl
 	});
 
+	// Refresh the nonce if login sends updated nonces over.
+	api.bind( 'nonce-refresh', function( nonces ) {
+		api.Widgets.data.nonce = nonces['update-widget'];
+	});
+
 	/**
 	 * Init Customizer for widgets.
 	 */
diff --git a/src/wp-includes/class-wp-customize-manager.php b/src/wp-includes/class-wp-customize-manager.php
index d24c283a4b..9fadd741c2 100644
--- a/src/wp-includes/class-wp-customize-manager.php
+++ b/src/wp-includes/class-wp-customize-manager.php
@@ -91,8 +91,8 @@ final class WP_Customize_Manager {
 
 		add_filter( 'wp_die_handler', array( $this, 'wp_die_handler' ) );
 
-		add_action( 'setup_theme',  array( $this, 'setup_theme' ) );
-		add_action( 'wp_loaded',    array( $this, 'wp_loaded' ) );
+		add_action( 'setup_theme', array( $this, 'setup_theme' ) );
+		add_action( 'wp_loaded',   array( $this, 'wp_loaded' ) );
 
 		// Run wp_redirect_status late to make sure we override the status last.
 		add_action( 'wp_redirect_status', array( $this, 'wp_redirect_status' ), 1000 );
@@ -105,7 +105,8 @@ final class WP_Customize_Manager {
 		remove_action( 'admin_init', '_maybe_update_plugins' );
 		remove_action( 'admin_init', '_maybe_update_themes' );
 
-		add_action( 'wp_ajax_customize_save', array( $this, 'save' ) );
+		add_action( 'wp_ajax_customize_save',           array( $this, 'save' ) );
+		add_action( 'wp_ajax_customize_refresh_nonces', array( $this, 'refresh_nonces' ) );
 
 		add_action( 'customize_register',                 array( $this, 'register_controls' ) );
 		add_action( 'customize_register',                 array( $this, 'register_dynamic_settings' ), 11 ); // allow code to create settings first
@@ -783,6 +784,34 @@ final class WP_Customize_Manager {
 		wp_send_json_success( $response );
 	}
 
+	/**
+	 * Refresh nonces for the current preview.
+	 *
+	 * @since 4.2.0
+	 */
+	public function refresh_nonces() {
+		if ( ! $this->is_preview() ) {
+			wp_send_json_error( 'not_preview' );
+		}
+
+		$nonces = array(
+			'save'    => wp_create_nonce( 'save-customize_' . $this->get_stylesheet() ),
+			'preview' => wp_create_nonce( 'preview-customize_' . $this->get_stylesheet() ),
+		);
+
+		/**
+		 * Filter nonces for a customize_refresh_nonces AJAX request.
+		 *
+		 * @since 4.2.0
+		 *
+		 * @param array                $nonces Array of refreshed nonces for save and
+		 *                                     preview actions.
+		 * @param WP_Customize_Manager $this   WP_Customize_Manager instance.
+		 */
+		$nonces = apply_filters( 'customize_refresh_nonces', $nonces, $this );
+		wp_send_json_success( $nonces );
+	}
+
 	/**
 	 * Add a customize setting.
 	 *
diff --git a/src/wp-includes/class-wp-customize-widgets.php b/src/wp-includes/class-wp-customize-widgets.php
index 966c853f9c..fe54d4cfd2 100644
--- a/src/wp-includes/class-wp-customize-widgets.php
+++ b/src/wp-includes/class-wp-customize-widgets.php
@@ -95,6 +95,7 @@ final class WP_Customize_Widgets {
 		add_action( 'customize_controls_print_footer_scripts', array( $this, 'print_footer_scripts' ) );
 		add_action( 'customize_controls_print_footer_scripts', array( $this, 'output_widget_control_templates' ) );
 		add_action( 'customize_preview_init',                  array( $this, 'customize_preview_init' ) );
+		add_filter( 'customize_refresh_nonces',                array( $this, 'refresh_nonces' ) );
 
 		add_action( 'dynamic_sidebar',                         array( $this, 'tally_rendered_widgets' ) );
 		add_filter( 'is_active_sidebar',                       array( $this, 'tally_sidebars_via_is_active_sidebar_calls' ), 10, 2 );
@@ -888,6 +889,20 @@ final class WP_Customize_Widgets {
 		add_action( 'wp_footer',          array( $this, 'export_preview_data' ), 20 );
 	}
 
+	/**
+	 * Refresh nonce for widget updates.
+	 *
+	 * @since 4.2.0
+	 * @access public
+	 *
+	 * @param  array $nonces Array of nonces.
+	 * @return array $nonces Array of nonces.
+	 */
+	public function refresh_nonces( $nonces ) {
+		$nonces['update-widget'] = wp_create_nonce( 'update-widget' );
+		return $nonces;
+	}
+
 	/**
 	 * When previewing, make sure the proper previewing widgets are used.
 	 *