diff --git a/src/wp-includes/connectors.php b/src/wp-includes/connectors.php
index 7811b3b7254d9..92c324cd2656d 100644
--- a/src/wp-includes/connectors.php
+++ b/src/wp-includes/connectors.php
@@ -547,7 +547,11 @@ function _wp_connectors_rest_settings_dispatch( WP_REST_Response $response, WP_R
 		// On update, validate AI provider keys before masking.
 		// Non-AI connectors accept keys as-is; the service plugin handles its own validation.
 		if ( $is_update && is_string( $value ) && '' !== $value && 'ai_provider' === $connector_data['type'] ) {
-			if ( true !== _wp_connectors_is_ai_api_key_valid( $value, $connector_id ) ) {
+			/*
+			 * Discard the key only when validation explicitly reports it as invalid.
+			 * Any other result preserves the stored key.
+			 */
+			if ( false === _wp_connectors_is_ai_api_key_valid( $value, $connector_id ) ) {
 				update_option( $setting_name, '' );
 				$data[ $setting_name ] = '';
 				continue;
diff --git a/tests/phpunit/tests/connectors/wpConnectorsRestSettingsDispatch.php b/tests/phpunit/tests/connectors/wpConnectorsRestSettingsDispatch.php
new file mode 100644
index 0000000000000..90355cb46c25f
--- /dev/null
+++ b/tests/phpunit/tests/connectors/wpConnectorsRestSettingsDispatch.php
@@ -0,0 +1,191 @@
+<?php
+
+require_once dirname( __DIR__, 2 ) . '/includes/wp-ai-client-mock-provider-trait.php';
+
+/**
+ * Tests for _wp_connectors_rest_settings_dispatch().
+ *
+ * @group connectors
+ * @group restapi
+ * @covers ::_wp_connectors_rest_settings_dispatch
+ */
+class Tests_Connectors_WpConnectorsRestSettingsDispatch extends WP_UnitTestCase {
+
+	use WP_AI_Client_Mock_Provider_Trait;
+
+	/**
+	 * The setting name for the registered mock AI provider connector.
+	 *
+	 * @var string
+	 */
+	private const MOCK_SETTING = 'connectors_ai_mock_connectors_test_api_key';
+
+	/**
+	 * A connector id registered as an AI provider but absent from the AI Client
+	 * registry, so its key can never be verified (validation returns null).
+	 *
+	 * @var string
+	 */
+	private const UNVERIFIABLE_ID = 'mock-connectors-unverifiable';
+
+	/**
+	 * The setting name for the unverifiable connector.
+	 *
+	 * @var string
+	 */
+	private const UNVERIFIABLE_SETTING = 'connectors_test_unverifiable_api_key';
+
+	/**
+	 * Registers the mock provider once before any tests in this class run.
+	 */
+	public static function set_up_before_class() {
+		parent::set_up_before_class();
+		self::register_mock_connectors_provider();
+	}
+
+	/**
+	 * Resets the mock availability flag and registers the unverifiable connector.
+	 */
+	public function set_up() {
+		parent::set_up();
+		self::set_mock_provider_configured( true );
+
+		$registry = WP_Connector_Registry::get_instance();
+		if ( null !== $registry && ! $registry->is_registered( self::UNVERIFIABLE_ID ) ) {
+			$registry->register(
+				self::UNVERIFIABLE_ID,
+				array(
+					'name'           => 'Mock Unverifiable',
+					'description'    => '',
+					'type'           => 'ai_provider',
+					'authentication' => array(
+						'method'       => 'api_key',
+						'setting_name' => self::UNVERIFIABLE_SETTING,
+					),
+				)
+			);
+		}
+	}
+
+	/**
+	 * Builds a POST request and response for the settings endpoint.
+	 *
+	 * @param string $setting_name The connector setting key.
+	 * @param string $value        The submitted/stored key value.
+	 * @return array{0: WP_REST_Response, 1: WP_REST_Request} The response and request.
+	 */
+	private function make_settings_update( string $setting_name, string $value ): array {
+		$request = new WP_REST_Request( 'POST', '/wp/v2/settings' );
+
+		$response = new WP_REST_Response( array( $setting_name => $value ) );
+
+		return array( $response, $request );
+	}
+
+	/**
+	 * A validation result that is not an explicit failure must preserve the stored key.
+	 *
+	 * @ticket 65551
+	 */
+	public function test_indeterminate_validation_preserves_key() {
+		$this->setExpectedIncorrectUsage( '_wp_connectors_is_ai_api_key_valid' );
+
+		update_option( self::UNVERIFIABLE_SETTING, 'existing-valid-key' );
+
+		list( $response, $request ) = $this->make_settings_update( self::UNVERIFIABLE_SETTING, 'existing-valid-key' );
+
+		$result = _wp_connectors_rest_settings_dispatch( $response, rest_get_server(), $request );
+
+		$this->assertSame(
+			'existing-valid-key',
+			get_option( self::UNVERIFIABLE_SETTING ),
+			'The stored key should be preserved when validation is indeterminate.'
+		);
+
+		$data = $result->get_data();
+		$this->assertNotSame(
+			'',
+			$data[ self::UNVERIFIABLE_SETTING ],
+			'The response value should not be emptied when validation is indeterminate.'
+		);
+	}
+
+	/**
+	 * An explicitly invalid key must be discarded.
+	 *
+	 * @ticket 65551
+	 */
+	public function test_invalid_key_is_discarded() {
+		self::set_mock_provider_configured( false );
+
+		update_option( self::MOCK_SETTING, 'bad-key' );
+
+		list( $response, $request ) = $this->make_settings_update( self::MOCK_SETTING, 'bad-key' );
+
+		$result = _wp_connectors_rest_settings_dispatch( $response, rest_get_server(), $request );
+
+		$this->assertSame(
+			'',
+			get_option( self::MOCK_SETTING ),
+			'An invalid key should be discarded.'
+		);
+
+		$data = $result->get_data();
+		$this->assertSame( '', $data[ self::MOCK_SETTING ] );
+	}
+
+	/**
+	 * A valid key must be preserved and masked in the response.
+	 *
+	 * @ticket 65551
+	 */
+	public function test_valid_key_is_preserved_and_masked() {
+		self::set_mock_provider_configured( true );
+
+		update_option( self::MOCK_SETTING, 'a-valid-secret-key' );
+
+		list( $response, $request ) = $this->make_settings_update( self::MOCK_SETTING, 'a-valid-secret-key' );
+
+		$result = _wp_connectors_rest_settings_dispatch( $response, rest_get_server(), $request );
+
+		$this->assertSame(
+			'a-valid-secret-key',
+			get_option( self::MOCK_SETTING ),
+			'A valid key should be preserved in the database.'
+		);
+
+		$data = $result->get_data();
+		$this->assertNotSame(
+			'a-valid-secret-key',
+			$data[ self::MOCK_SETTING ],
+			'The raw key should never be exposed in the response.'
+		);
+		$this->assertStringEndsWith(
+			'-key',
+			$data[ self::MOCK_SETTING ],
+			'The masked value should retain the final characters of the key.'
+		);
+	}
+
+	/**
+	 * Read (GET) requests must never validate or discard the stored key.
+	 *
+	 * @ticket 65551
+	 */
+	public function test_get_request_does_not_discard_key() {
+		self::set_mock_provider_configured( false );
+
+		update_option( self::MOCK_SETTING, 'a-valid-secret-key' );
+
+		$request  = new WP_REST_Request( 'GET', '/wp/v2/settings' );
+		$response = new WP_REST_Response( array( self::MOCK_SETTING => 'a-valid-secret-key' ) );
+
+		_wp_connectors_rest_settings_dispatch( $response, rest_get_server(), $request );
+
+		$this->assertSame(
+			'a-valid-secret-key',
+			get_option( self::MOCK_SETTING ),
+			'A GET request must not discard the stored key, even for an unconfigured provider.'
+		);
+	}
+}