diff --git a/src/wp-includes/abilities-api/class-wp-ability.php b/src/wp-includes/abilities-api/class-wp-ability.php
index 967f1641156b0..cc01cc274c143 100644
--- a/src/wp-includes/abilities-api/class-wp-ability.php
+++ b/src/wp-includes/abilities-api/class-wp-ability.php
@@ -502,7 +502,7 @@ public function validate_input( $input = null ) {
 	 *
 	 * @param callable $callback The callable to invoke.
 	 * @param mixed    $input    Optional. The input data for the ability. Default `null`.
-	 * @return mixed The result of the callable execution.
+	 * @return mixed The result of the callable execution, or a `WP_Error` if the callback threw.
 	 */
 	protected function invoke_callback( callable $callback, $input = null ) {
 		$args = array();
@@ -510,7 +510,19 @@ protected function invoke_callback( callable $callback, $input = null ) {
 			$args[] = $input;
 		}
 
-		return $callback( ...$args );
+		try {
+			return $callback( ...$args );
+		} catch ( Throwable $e ) {
+			return new WP_Error(
+				'ability_callback_exception',
+				sprintf(
+					/* translators: 1: Ability name, 2: Exception message. */
+					__( 'Ability "%1$s" callback threw an exception: %2$s' ),
+					esc_html( $this->name ),
+					esc_html( $e->getMessage() )
+				)
+			);
+		}
 	}
 
 	/**
diff --git a/tests/phpunit/tests/abilities-api/wpAbility.php b/tests/phpunit/tests/abilities-api/wpAbility.php
index 73a5fbf17a9ef..aea2c09624929 100644
--- a/tests/phpunit/tests/abilities-api/wpAbility.php
+++ b/tests/phpunit/tests/abilities-api/wpAbility.php
@@ -497,6 +497,54 @@ public function test_execute_no_input() {
 		$this->assertSame( 42, $ability->execute() );
 	}
 
+	/**
+	 * Tests that an exception thrown by the execute callback is converted to a WP_Error
+	 * instead of being propagated as an uncaught throwable.
+	 *
+	 * @ticket 65058
+	 */
+	public function test_execute_catches_callback_exception() {
+		$args = array_merge(
+			self::$test_ability_properties,
+			array(
+				'execute_callback' => static function (): int {
+					throw new RuntimeException( 'boom' );
+				},
+			)
+		);
+
+		$ability = new WP_Ability( self::$test_ability_name, $args );
+		$result  = $ability->execute();
+
+		$this->assertWPError( $result, 'Ability::execute() should return WP_Error when the callback throws.' );
+		$this->assertSame( 'ability_callback_exception', $result->get_error_code() );
+		$this->assertStringContainsString( 'boom', $result->get_error_message() );
+	}
+
+	/**
+	 * Tests that an exception thrown by the permission callback is converted to a WP_Error
+	 * instead of being propagated as an uncaught throwable.
+	 *
+	 * @ticket 65058
+	 */
+	public function test_check_permissions_catches_callback_exception() {
+		$args = array_merge(
+			self::$test_ability_properties,
+			array(
+				'permission_callback' => static function (): bool {
+					throw new RuntimeException( 'permission exploded' );
+				},
+			)
+		);
+
+		$ability = new WP_Ability( self::$test_ability_name, $args );
+		$result  = $ability->check_permissions();
+
+		$this->assertWPError( $result, 'Ability::check_permissions() should return WP_Error when the callback throws.' );
+		$this->assertSame( 'ability_callback_exception', $result->get_error_code() );
+		$this->assertStringContainsString( 'permission exploded', $result->get_error_message() );
+	}
+
 	/**
 	 * Tests that before_execute_ability action is fired with correct parameters.
 	 *