diff --git a/src/wp-includes/abilities-api/class-wp-ability.php b/src/wp-includes/abilities-api/class-wp-ability.php
index d116080c1ccdc..3af7f7fc9844e 100644
--- a/src/wp-includes/abilities-api/class-wp-ability.php
+++ b/src/wp-includes/abilities-api/class-wp-ability.php
@@ -277,13 +277,15 @@ protected function prepare_properties( array $args ): array {
 			);
 		}
 
-		if ( empty( $args['execute_callback'] ) || ! is_callable( $args['execute_callback'] ) ) {
+		// If we are not overriding `ability_class` parameter during instantiation, then we need to validate the execute_callback.
+		if ( get_class( $this ) === self::class && ( empty( $args['execute_callback'] ) || ! is_callable( $args['execute_callback'] ) ) ) {
 			throw new InvalidArgumentException(
 				__( 'The ability properties must contain a valid `execute_callback` function.' )
 			);
 		}
 
-		if ( empty( $args['permission_callback'] ) || ! is_callable( $args['permission_callback'] ) ) {
+		// If we are not overriding `ability_class` parameter during instantiation, then we need to validate the permission_callback.
+		if ( get_class( $this ) === self::class && ( empty( $args['permission_callback'] ) || ! is_callable( $args['permission_callback'] ) ) ) {
 			throw new InvalidArgumentException(
 				__( 'The ability properties must provide a valid `permission_callback` function.' )
 			);
diff --git a/tests/phpunit/includes/class-tests-custom-ability-class.php b/tests/phpunit/includes/class-tests-custom-ability-class.php
new file mode 100644
index 0000000000000..6e600e5c013e1
--- /dev/null
+++ b/tests/phpunit/includes/class-tests-custom-ability-class.php
@@ -0,0 +1,29 @@
+<?php
+/**
+ * Test custom ability class that extends WP_Ability.
+ *
+ * This class overrides do_execute() and check_permissions() directly,
+ * allowing registration without execute_callback or permission_callback.
+ */
+class Tests_Custom_Ability_Class extends WP_Ability {
+
+	/**
+	 * Custom execute implementation that multiplies instead of adds.
+	 *
+	 * @param mixed $input The input data.
+	 * @return int The result of multiplying a and b.
+	 */
+	protected function do_execute( $input = null ) {
+		return $input['a'] * $input['b'];
+	}
+
+	/**
+	 * Custom permission check that always returns true.
+	 *
+	 * @param mixed $input The input data.
+	 * @return bool Always true.
+	 */
+	public function check_permissions( $input = null ) {
+		return true;
+	}
+}
diff --git a/tests/phpunit/tests/abilities-api/wpAbilitiesRegistry.php b/tests/phpunit/tests/abilities-api/wpAbilitiesRegistry.php
index 319063196d0c5..32479d69e2f8c 100644
--- a/tests/phpunit/tests/abilities-api/wpAbilitiesRegistry.php
+++ b/tests/phpunit/tests/abilities-api/wpAbilitiesRegistry.php
@@ -23,6 +23,8 @@ class Tests_Abilities_API_WpAbilitiesRegistry extends WP_UnitTestCase {
 	 * Set up each test method.
 	 */
 	public function set_up(): void {
+		require_once DIR_TESTDATA . '/../includes/class-tests-custom-ability-class.php';
+
 		parent::set_up();
 
 		$this->registry = new WP_Abilities_Registry();
@@ -257,6 +259,36 @@ public function test_register_incorrect_execute_callback_type() {
 		$this->assertNull( $result );
 	}
 
+	/**
+	 * Should allow ability registration with custom ability_class that overrides do_execute.
+	 *
+	 * @ticket 64407
+	 *
+	 * @covers WP_Abilities_Registry::register
+	 * @covers WP_Ability::prepare_properties
+	 */
+	public function test_register_with_custom_ability_class_without_execute_callback() {
+		// Remove execute_callback and permission_callback since the custom class provides its own implementation.
+		unset( self::$test_ability_args['execute_callback'] );
+		unset( self::$test_ability_args['permission_callback'] );
+
+		self::$test_ability_args['ability_class'] = 'Tests_Custom_Ability_Class';
+
+		$result = $this->registry->register( self::$test_ability_name, self::$test_ability_args );
+
+		$this->assertInstanceOf( WP_Ability::class, $result, 'Should return a WP_Ability instance.' );
+		$this->assertInstanceOf( Tests_Custom_Ability_Class::class, $result, 'Should return an instance of the custom class.' );
+
+		// Verify the custom execute method works.
+		$execute_result = $result->execute(
+			array(
+				'a' => 5,
+				'b' => 3,
+			)
+		);
+		$this->assertSame( 15, $execute_result, 'Custom do_execute should multiply instead of add.' );
+	}
+
 	/**
 	 * Should reject ability registration without an execute callback.
 	 *