diff --git a/tests/phpunit/tests/admin/includes/ajax-actions/updateWidget.php b/tests/phpunit/tests/admin/includes/ajax-actions/updateWidget.php
new file mode 100644
index 0000000000000..8dde018d15382
--- /dev/null
+++ b/tests/phpunit/tests/admin/includes/ajax-actions/updateWidget.php
@@ -0,0 +1,117 @@
+<?php
+
+/**
+ * Admin Ajax functions to be tested.
+ */
+require_once ABSPATH . 'wp-admin/includes/ajax-actions.php';
+
+/**
+ * Testing wp_ajax_update_widget() functionality.
+ *
+ * @package WordPress
+ * @subpackage UnitTests
+ * @since 3.9.0
+ *
+ * @group ajax
+ *
+ * @covers ::wp_ajax_update_widget
+ */
+class Tests_wp_ajax_update_widget extends WP_Ajax_UnitTestCase {
+
+	/**
+	 * Administrator user ID.
+	 *
+	 * @var int
+	 */
+	protected static $admin_id;
+
+	/**
+	 * Setup test fixtures.
+	 *
+	 * @param WP_UnitTest_Factory $factory
+	 */
+	public static function wpSetUpBeforeClass( WP_UnitTest_Factory $factory ): void {
+		self::$admin_id = $factory->user->create( array( 'role' => 'administrator' ) );
+	}
+
+	public function set_up() {
+		parent::set_up();
+		// Initialize the Customizer.
+		require_once ABSPATH . WPINC . '/class-wp-customize-manager.php';
+		$GLOBALS['wp_customize'] = new WP_Customize_Manager();
+	}
+
+	/**
+	 * Tests failure due to invalid nonce.
+	 *
+	 * @ticket 65252
+	 */
+	public function test_update_widget_invalid_nonce(): void {
+		wp_set_current_user( self::$admin_id );
+
+		$_POST = array(
+			'action' => 'update-widget',
+			'nonce'  => 'invalid-nonce',
+		);
+
+		$this->expectException( WPAjaxDieStopException::class );
+		$this->expectExceptionMessage( '-1' );
+
+		$this->_handleAjax( 'update-widget' );
+	}
+
+	/**
+	 * Tests failure due to missing widget-id.
+	 *
+	 * @ticket 65252
+	 */
+	public function test_update_widget_missing_widget_id(): void {
+		wp_set_current_user( self::$admin_id );
+
+		$_POST = array(
+			'action' => 'update-widget',
+			'nonce'  => wp_create_nonce( 'update-widget' ),
+		);
+
+		try {
+			$this->_handleAjax( 'update-widget' );
+		} catch ( WPAjaxDieStopException $e ) {
+			$this->_last_response = $e->getMessage();
+		} catch ( WPAjaxDieContinueException $e ) {
+		}
+
+		$response = json_decode( $this->_last_response, true );
+		$this->assertFalse( $response['success'] );
+		$this->assertSame( 'missing_widget-id', $response['data'] );
+	}
+
+	/**
+	 * Tests failure for template widget.
+	 *
+	 * @ticket 65252
+	 */
+	public function test_update_widget_template_widget_not_updatable(): void {
+		wp_set_current_user( self::$admin_id );
+
+		$id_base   = 'text';
+		$widget_id = $id_base . '-1';
+
+		$_POST = array(
+			'action'             => 'update-widget',
+			'nonce'              => wp_create_nonce( 'update-widget' ),
+			'widget-id'          => $widget_id,
+			'widget-' . $id_base => array( '__i__' => array( 'title' => 'Title' ) ),
+		);
+
+		try {
+			$this->_handleAjax( 'update-widget' );
+		} catch ( WPAjaxDieStopException $e ) {
+			$this->_last_response = $e->getMessage();
+		} catch ( WPAjaxDieContinueException $e ) {
+		}
+
+		$response = json_decode( $this->_last_response, true );
+		$this->assertFalse( $response['success'], 'Should fail for template widget' );
+		$this->assertSame( 'template_widget_not_updatable', $response['data'] );
+	}
+}