diff --git a/src/wp-admin/includes/class-wp-upgrader.php b/src/wp-admin/includes/class-wp-upgrader.php
index ba27113ff73de..d5eeae81afd98 100644
--- a/src/wp-admin/includes/class-wp-upgrader.php
+++ b/src/wp-admin/includes/class-wp-upgrader.php
@@ -746,6 +746,8 @@ public function install_package( $args = array() ) {
 	 *
 	 * @since 2.8.0
 	 *
+	 * @global WP_Filesystem_Base $wp_filesystem WordPress filesystem subclass.
+	 *
 	 * @param array $options {
 	 *     Array or string of arguments for upgrading/installing a package.
 	 *
@@ -772,6 +774,7 @@ public function install_package( $args = array() ) {
 	 *                              or false if unable to connect to the filesystem.
 	 */
 	public function run( $options ) {
+		global $wp_filesystem;
 
 		$defaults = array(
 			'package'                     => '', // Please always pass this.
@@ -906,6 +909,13 @@ public function run( $options ) {
 			)
 		);
 
+		if ( is_wp_error( $result ) && $options['clear_working']
+			&& $wp_filesystem instanceof WP_Filesystem_Base
+			&& $wp_filesystem->exists( $working_dir )
+		) {
+			$wp_filesystem->delete( $working_dir, true );
+		}
+
 		/**
 		 * Filters the result of WP_Upgrader::install_package().
 		 *
diff --git a/tests/phpunit/tests/admin/wpUpgrader.php b/tests/phpunit/tests/admin/wpUpgrader.php
index ffea594ae87bc..bce2f916910d2 100644
--- a/tests/phpunit/tests/admin/wpUpgrader.php
+++ b/tests/phpunit/tests/admin/wpUpgrader.php
@@ -1464,6 +1464,62 @@ public function test_run_should_return_false_when_requesting_filesystem_credenti
 		$this->assertFalse( self::$instance->run( array() ) );
 	}
 
+	/**
+	 * Tests that `WP_Upgrader::run()` removes the working directory after an
+	 * installation failure.
+	 *
+	 * @ticket 44710
+	 *
+	 * @covers WP_Upgrader::run
+	 */
+	public function test_run_should_clear_working_directory_after_installation_failure() {
+		$working_directory = '/wp-content/upgrade/test-package';
+		$expected          = new WP_Error( 'incompatible_archive' );
+
+		self::$wp_filesystem_mock
+				->expects( $this->once() )
+				->method( 'exists' )
+				->with( $working_directory )
+				->willReturn( true );
+
+		self::$wp_filesystem_mock
+				->expects( $this->once() )
+				->method( 'delete' )
+				->with( $working_directory, true );
+		// Note: setMethods() is deprecated in PHPUnit 9, but still supported.
+		$instance = $this->getMockBuilder( 'WP_Upgrader' )
+				->setConstructorArgs( array( self::$upgrader_skin_mock ) )
+				->setMethods( array( 'fs_connect', 'download_package', 'unpack_package', 'install_package' ) )
+				->getMock();
+
+		$instance
+				->method( 'fs_connect' )
+				->willReturn( true );
+
+		$instance
+				->method( 'download_package' )
+				->willReturn( '/tmp/test-package.zip' );
+
+		$instance
+				->method( 'unpack_package' )
+				->willReturn( $working_directory );
+
+		$instance
+				->method( 'install_package' )
+				->willReturn( $expected );
+
+		$actual = $instance->run(
+			array(
+				'package'       => '/tmp/test-package.zip',
+				'destination'   => WP_PLUGIN_DIR,
+				'clear_working' => true,
+				'is_multi'      => true,
+			)
+		);
+
+		$this->assertSame( $expected, $actual );
+	}
+
 	/**
 	 * Tests that `WP_Upgrader::maintenance_mode()` removes the `.maintenance` file.
 	 *