diff --git a/includes/Checker/AJAX_Runner.php b/includes/Checker/AJAX_Runner.php
new file mode 100644
index 000000000..eb46bc0df
--- /dev/null
+++ b/includes/Checker/AJAX_Runner.php
@@ -0,0 +1,88 @@
+<?php
+/**
+ * Class WordPress\Plugin_Check\Checker\AJAX_Runner
+ *
+ * @package plugin-check
+ */
+
+namespace WordPress\Plugin_Check\Checker;
+
+use Exception;
+use WordPress\Plugin_Check\Utilities\Plugin_Request_Utility;
+
+/**
+ * AJAX Runner class.
+ *
+ * @since n.e.x.t
+ */
+class AJAX_Runner extends Abstract_Check_Runner {
+
+	/**
+	 * An instance of the Checks class.
+	 *
+	 * @since n.e.x.t
+	 * @var Checks
+	 */
+	protected $checks;
+
+	/**
+	 * Checks if the current request is an AJAX request for the Plugin Checker.
+	 *
+	 * @since n.e.x.t
+	 *
+	 * @return bool Returns true if is an AJAX request for the plugin check else false.
+	 */
+	public function is_plugin_check() {
+		if ( ! wp_doing_ajax() ) {
+			return false;
+		}
+
+		if ( ! isset( $_REQUEST['action'] ) || 'plugin_check_run_checks' !== $_REQUEST['action'] ) {
+			return false;
+		}
+
+		return true;
+	}
+
+	/**
+	 * Creates and returns an instance of the Checks class based on the request.
+	 *
+	 * @since n.e.x.t
+	 *
+	 * @return Checks An instance of the Checks class.
+	 *
+	 * @throws Exception Thrown if the plugin main file cannot be found based on the AJAX input.
+	 */
+	protected function get_checks_instance() {
+		if ( ! isset( $this->checks ) ) {
+			if ( ! isset( $_REQUEST['plugin'] ) ) {
+				throw new Exception( 'Invalid plugin slug: Plugin slug must not be empty.' );
+			}
+
+			// Get the plugin name from the AJAX request.
+			$plugin_file = Plugin_Request_Utility::get_plugin_basename_from_input( $_REQUEST['plugin'] );
+
+			$this->checks = new Checks( WP_PLUGIN_DIR . '/' . $plugin_file );
+		}
+
+		return $this->checks;
+	}
+
+	/**
+	 * Returns an array of Check slugs to run based on the request.
+	 *
+	 * @since n.e.x.t
+	 *
+	 * @return array An array of Check slugs to run.
+	 */
+	protected function get_check_slugs_to_run() {
+		$checks = array();
+
+		if ( isset( $_REQUEST['checks'] ) ) {
+			// Checks are passed as a comma separated string.
+			$checks = wp_parse_list( $_REQUEST['checks'] );
+		}
+
+		return $checks;
+	}
+}
diff --git a/includes/Checker/Abstract_Check_Runner.php b/includes/Checker/Abstract_Check_Runner.php
index d3d44c6ce..b1762344a 100644
--- a/includes/Checker/Abstract_Check_Runner.php
+++ b/includes/Checker/Abstract_Check_Runner.php
@@ -30,7 +30,7 @@ abstract public function is_plugin_check();
 	 *
 	 * @since n.e.x.t
 	 *
-	 * @return Checks An instances of the Checks class.
+	 * @return Checks An instance of the Checks class.
 	 */
 	abstract protected function get_checks_instance();
 
diff --git a/includes/Checker/CLI_Runner.php b/includes/Checker/CLI_Runner.php
index d240ebf2c..a084b61ae 100644
--- a/includes/Checker/CLI_Runner.php
+++ b/includes/Checker/CLI_Runner.php
@@ -17,7 +17,7 @@
 class CLI_Runner extends Abstract_Check_Runner {
 
 	/**
-	 * An instances of the Checks class.
+	 * An instance of the Checks class.
 	 *
 	 * @since n.e.x.t
 	 * @var Checks
@@ -29,7 +29,7 @@ class CLI_Runner extends Abstract_Check_Runner {
 	 *
 	 * @since n.e.x.t
 	 *
-	 * @return bool
+	 * @return bool Returns true if is an CLI request for the plugin check else false.
 	 */
 	public function is_plugin_check() {
 		if ( empty( $_SERVER['argv'] ) || 3 > count( $_SERVER['argv'] ) ) {
@@ -48,11 +48,11 @@ public function is_plugin_check() {
 	}
 
 	/**
-	 * Retruns an instance of the Checks class.
+	 * Creates and returns an instance of the Checks class based on the request.
 	 *
 	 * @since n.e.x.t
 	 *
-	 * @return Checks
+	 * @return Checks An instance of the Checks class.
 	 *
 	 * @throws Exception Thrown if the plugin main file cannot be found based on the CLI input.
 	 */
@@ -69,11 +69,11 @@ protected function get_checks_instance() {
 	}
 
 	/**
-	 * Returns an array of Check instances to run.
+	 * Returns an array of Check slugs to run based on the request.
 	 *
 	 * @since n.e.x.t
 	 *
-	 * @return array An array of Check instances to run.
+	 * @return array An array of Check slugs to run.
 	 */
 	protected function get_check_slugs_to_run() {
 		$checks = array();
diff --git a/tests/Checker/AJAX_Runner_Tests.php b/tests/Checker/AJAX_Runner_Tests.php
new file mode 100644
index 000000000..52a4160c3
--- /dev/null
+++ b/tests/Checker/AJAX_Runner_Tests.php
@@ -0,0 +1,153 @@
+<?php
+/**
+ * Tests for the Checks class.
+ *
+ * @package plugin-check
+ */
+
+use WordPress\Plugin_Check\Checker\AJAX_Runner;
+use WordPress\Plugin_Check\Checker\Check_Result;
+
+class AJAX_Runner_Tests extends WP_UnitTestCase {
+
+	public function test_is_plugin_check_returns_true() {
+		// Mock the AJAX request.
+		add_filter( 'wp_doing_ajax', '__return_true' );
+		$_REQUEST['action'] = 'plugin_check_run_checks';
+
+		$runner = new AJAX_Runner();
+
+		$this->assertTrue( $runner->is_plugin_check() );
+	}
+
+	public function test_is_plugin_check_returns_false() {
+		// Mock the AJAX request.
+		add_filter( 'wp_doing_ajax', '__return_true' );
+		$_REQUEST['action'] = 'a_different_ajax_request';
+
+		$runner = new AJAX_Runner();
+
+		$this->assertFalse( $runner->is_plugin_check() );
+	}
+
+	public function test_is_plugin_check_returns_false_not_ajax() {
+		// Mock the AJAX request.
+		add_filter( 'wp_doing_ajax', '__return_false' );
+
+		$runner = new AJAX_Runner();
+
+		$this->assertFalse( $runner->is_plugin_check() );
+	}
+
+	public function test_prepare_with_runtime_check() {
+		add_filter( 'wp_doing_ajax', '__return_true' );
+		$_REQUEST['action'] = 'plugin_check_run_checks';
+		$_REQUEST['plugin'] = 'plugin-check';
+		$_REQUEST['checks'] = 'runtime_check';
+
+		add_filter(
+			'wp_plugin_check_checks',
+			function( $checks ) {
+				return array(
+					'runtime_check' => new WordPress\Plugin_Check\Test_Data\Runtime_Check(),
+				);
+			}
+		);
+
+		$runner  = new AJAX_Runner();
+		$cleanup = $runner->prepare();
+
+		$this->assertIsCallable( $cleanup );
+
+		// Assert the Universal_Runtume_Preparation was run.
+		$this->assertTrue( has_filter( 'option_active_plugins' ) );
+		$this->assertTrue( has_filter( 'default_option_active_plugins' ) );
+		$this->assertTrue( has_filter( 'stylesheet' ) );
+		$this->assertTrue( has_filter( 'template' ) );
+		$this->assertTrue( has_filter( 'pre_option_template' ) );
+		$this->assertTrue( has_filter( 'pre_option_stylesheet' ) );
+		$this->assertTrue( has_filter( 'pre_option_current_theme' ) );
+		$this->assertTrue( has_filter( 'pre_option_template_root' ) );
+		$this->assertTrue( has_filter( 'pre_option_stylesheet_root' ) );
+	}
+
+	public function test_prepare_with_static_check() {
+		add_filter( 'wp_doing_ajax', '__return_true' );
+		$_REQUEST['action'] = 'plugin_check_run_checks';
+		$_REQUEST['plugin'] = 'plugin-check';
+		$_REQUEST['checks'] = 'empty_check';
+
+		add_filter(
+			'wp_plugin_check_checks',
+			function( $checks ) {
+				return array(
+					'empty_check' => new WordPress\Plugin_Check\Test_Data\Empty_Check(),
+				);
+			}
+		);
+
+		$runner  = new AJAX_Runner();
+		$cleanup = $runner->prepare();
+
+		$this->assertIsCallable( $cleanup );
+
+		// Assert the Universal_Runtume_Preparation was not run.
+		$this->assertFalse( has_filter( 'option_active_plugins' ) );
+		$this->assertFalse( has_filter( 'default_option_active_plugins' ) );
+		$this->assertFalse( has_filter( 'stylesheet' ) );
+		$this->assertFalse( has_filter( 'template' ) );
+		$this->assertFalse( has_filter( 'pre_option_template' ) );
+		$this->assertFalse( has_filter( 'pre_option_stylesheet' ) );
+		$this->assertFalse( has_filter( 'pre_option_current_theme' ) );
+		$this->assertFalse( has_filter( 'pre_option_template_root' ) );
+		$this->assertFalse( has_filter( 'pre_option_stylesheet_root' ) );
+	}
+
+	public function test_run() {
+		add_filter( 'wp_doing_ajax', '__return_true' );
+		$_REQUEST['action'] = 'plugin_check_run_checks';
+		$_REQUEST['plugin'] = 'plugin-check';
+		$_REQUEST['checks'] = 'empty_check';
+
+		add_filter(
+			'wp_plugin_check_checks',
+			function( $checks ) {
+				return array(
+					'empty_check' => new WordPress\Plugin_Check\Test_Data\Empty_Check(),
+				);
+			}
+		);
+
+		$runner = new AJAX_Runner();
+		$runner->prepare();
+		$results = $runner->run();
+
+		$this->assertInstanceOf( Check_Result::class, $results );
+		$this->assertEmpty( $results->get_warnings() );
+		$this->assertEmpty( $results->get_errors() );
+	}
+
+	public function test_run_with_errors() {
+		add_filter( 'wp_doing_ajax', '__return_true' );
+		$_REQUEST['action'] = 'plugin_check_run_checks';
+		$_REQUEST['plugin'] = 'plugin-check';
+		$_REQUEST['checks'] = 'error_check';
+
+		add_filter(
+			'wp_plugin_check_checks',
+			function( $checks ) {
+				return array(
+					'error_check' => new WordPress\Plugin_Check\Test_Data\Error_Check(),
+				);
+			}
+		);
+
+		$runner = new AJAX_Runner();
+		$runner->prepare();
+		$results = $runner->run();
+
+		$this->assertInstanceOf( Check_Result::class, $results );
+		$this->assertEmpty( $results->get_warnings() );
+		$this->assertNotEmpty( $results->get_errors() );
+	}
+}