diff --git a/tests/phpunit/tests/admin/includes/ajax-actions/autocompleteUser.php b/tests/phpunit/tests/admin/includes/ajax-actions/autocompleteUser.php
new file mode 100644
index 0000000000000..a73bba4879757
--- /dev/null
+++ b/tests/phpunit/tests/admin/includes/ajax-actions/autocompleteUser.php
@@ -0,0 +1,151 @@
+<?php
+
+/**
+ * Admin Ajax functions to be tested.
+ */
+require_once ABSPATH . 'wp-admin/includes/ajax-actions.php';
+
+/**
+ * Testing wp_ajax_autocomplete_user() functionality.
+ *
+ * @package WordPress
+ * @subpackage UnitTests
+ * @since 3.4.0
+ *
+ * @group ajax
+ *
+ * @covers ::wp_ajax_autocomplete_user
+ */
+class Tests_wp_ajax_autocomplete_user extends WP_Ajax_UnitTestCase {
+
+	/**
+	 * User ID of a test user.
+	 *
+	 * @var int
+	 */
+	protected static $user_id;
+
+	/**
+	 * Setup test fixtures.
+	 */
+	public static function wpSetUpBeforeClass( WP_UnitTest_Factory $factory ): void {
+		self::$user_id = $factory->user->create(
+			array(
+				'user_login' => 'testuser',
+				'user_email' => 'testuser@example.com',
+				'first_name' => 'Test',
+				'last_name'  => 'User',
+			)
+		);
+	}
+
+	/**
+	 * Tests user autocomplete via AJAX.
+	 *
+	 * @ticket 65252
+	 *
+	 * @dataProvider data_autocomplete_user
+	 *
+	 * @param array $request_params Request parameters.
+	 * @param array $expected       Expected results.
+	 * @param bool  $is_member      Whether the user should be a member of the blog.
+	 */
+	public function test_autocomplete_user( array $request_params, array $expected, bool $is_member = true ): void {
+		if ( ! is_multisite() ) {
+			$this->markTestSkipped( 'wp_ajax_autocomplete_user() is multisite only.' );
+		}
+
+		// Mock the user with necessary capabilities.
+		$this->_setRole( 'administrator' );
+		wp_set_current_user( self::$user_id );
+		grant_super_admin( self::$user_id );
+
+		if ( ! $is_member ) {
+			remove_user_from_blog( self::$user_id, get_current_blog_id() );
+		} else {
+			add_user_to_blog( get_current_blog_id(), self::$user_id, 'subscriber' );
+		}
+
+		$_GET     = array_merge( $_GET, $request_params );
+		$_POST    = array_merge( $_POST, $request_params );
+		$_REQUEST = array_merge( $_REQUEST, $request_params );
+
+		try {
+			add_action( 'admin_init', 'wp_ajax_autocomplete_user', 1 );
+			$this->_handleAjax( 'autocomplete_user' );
+		} catch ( WPAjaxDieContinueException $e ) {
+			$this->_last_response = (string) $e->getMessage();
+		} catch ( WPAjaxDieStopException $e ) {
+			$this->_last_response = (string) $e->getMessage();
+		}
+
+		$response = json_decode( $this->_last_response, true );
+
+		$this->assertIsArray( $response, 'Response should be a JSON array' );
+
+		foreach ( $expected as $index => $expected_item ) {
+			$this->assertArrayHasKey( $index, $response, "Response should have index $index" );
+			$this->assertSame( $expected_item['label'], $response[ $index ]['label'], "Label mismatch at index $index" );
+			$this->assertSame( $expected_item['value'], $response[ $index ]['value'], "Value mismatch at index $index" );
+		}
+	}
+
+	/**
+	 * Data provider for test_autocomplete_user.
+	 *
+	 * @return array<string, array{
+	 *     request_params: array,
+	 *     expected: array,
+	 *     is_member?: bool,
+	 * }>
+	 */
+	public function data_autocomplete_user(): array {
+		return array(
+			'search by login'                   => array(
+				'request_params' => array(
+					'term'              => 'testuser',
+					'autocomplete_type' => 'search',
+				),
+				'expected'       => array(
+					array(
+						'label' => 'testuser (testuser@example.com)',
+						'value' => 'testuser',
+					),
+				),
+			),
+			'add by login (exclude existing)'   => array(
+				'request_params' => array(
+					'term'              => 'testuser',
+					'autocomplete_type' => 'add',
+				),
+				'expected'       => array(),
+			),
+			'add by login (include non-member)' => array(
+				'request_params' => array(
+					'term'              => 'testuser',
+					'autocomplete_type' => 'add',
+				),
+				'expected'       => array(
+					array(
+						'label' => 'testuser (testuser@example.com)',
+						'value' => 'testuser',
+					),
+				),
+				'is_member'      => false,
+			),
+			'search by email'                   => array(
+				'request_params' => array(
+					'term'               => 'testuser@example.com',
+					'autocomplete_type'  => 'search',
+					'autocomplete_field' => 'user_email',
+				),
+				'expected'       => array(
+					array(
+						'label' => 'testuser (testuser@example.com)',
+						'value' => 'testuser@example.com',
+					),
+				),
+			),
+		);
+	}
+}