diff --git a/src/wp-includes/ai-client/class-wp-ai-client-prompt-builder.php b/src/wp-includes/ai-client/class-wp-ai-client-prompt-builder.php
index a64957fe73157..81297aced2571 100644
--- a/src/wp-includes/ai-client/class-wp-ai-client-prompt-builder.php
+++ b/src/wp-includes/ai-client/class-wp-ai-client-prompt-builder.php
@@ -43,7 +43,9 @@
  * interface. As soon as any exception is caught in a chain of method calls,
  * the returned instance will be in an error state, and all subsequent method
  * calls will be no-ops that just return the same error state instance. Only
- * when a generating method is called, the WP_Error will be returned.
+ * when a generating method is called, the WP_Error will be returned. The
+ * support check methods are the exception to the no-op behavior: they return
+ * false rather than the error state instance.
  *
  * @since 7.0.0
  *
@@ -79,7 +81,7 @@
  * @method self as_output_media_aspect_ratio(string $aspectRatio) Sets the output media aspect ratio.
  * @method self as_output_speech_voice(string $voice) Sets the output speech voice.
  * @method self as_json_response(?array<string, mixed> $schema = null) Configures the prompt for JSON response output.
- * @method bool|WP_Error is_supported(?CapabilityEnum $capability = null) Checks if the prompt is supported for the given capability.
+ * @method bool is_supported(?CapabilityEnum $capability = null) Checks if the prompt is supported for the given capability.
  * @method bool is_supported_for_text_generation() Checks if the prompt is supported for text generation.
  * @method bool is_supported_for_image_generation() Checks if the prompt is supported for image generation.
  * @method bool is_supported_for_text_to_speech_conversion() Checks if the prompt is supported for text to speech conversion.
@@ -282,7 +284,7 @@ public function using_abilities( ...$abilities ): self {
 	 *
 	 * This allows WordPress developers to use snake_case naming conventions. It catches
 	 * any exceptions thrown, stores them, and returns a WP_Error when a terminate method
-	 * is called.
+	 * is called, or false when a support check method is called.
 	 *
 	 * @since 7.0.0
 	 *
@@ -364,6 +366,9 @@ public function __call( string $name, array $arguments ) {
 			if ( self::is_generating_method( $name ) ) {
 				return $this->error;
 			}
+			if ( self::is_support_check_method( $name ) ) {
+				return false;
+			}
 			return $this;
 		}
 	}
diff --git a/tests/phpunit/tests/ai-client/wpAiClientPromptBuilder.php b/tests/phpunit/tests/ai-client/wpAiClientPromptBuilder.php
index 0669be8cc7bb4..bec6f6fcad8e2 100644
--- a/tests/phpunit/tests/ai-client/wpAiClientPromptBuilder.php
+++ b/tests/phpunit/tests/ai-client/wpAiClientPromptBuilder.php
@@ -2648,6 +2648,88 @@ public function test_support_check_methods_return_false_in_error_state() {
 		$this->assertFalse( $prompt_builder->is_supported_for_text_generation(), 'is_supported_for_text_generation should return false when in error state' );
 	}
 
+	/**
+	 * Tests that support check methods return false when the wrapped builder throws.
+	 *
+	 * @ticket 65781
+	 *
+	 * @dataProvider data_support_check_methods
+	 *
+	 * @param string $method         The support check method on the wrapper.
+	 * @param string $wrapped_method The matching method on the wrapped builder.
+	 */
+	public function test_support_check_methods_return_false_when_builder_throws( $method, $wrapped_method ) {
+		$registry       = AiClient::defaultRegistry();
+		$prompt_builder = new WP_AI_Client_Prompt_Builder( $registry, 'Test text' );
+
+		$wrapped_builder = $this->createMock( PromptBuilder::class );
+		$wrapped_builder->method( $wrapped_method )
+			->willThrowException( new RuntimeException( 'Thrown by the wrapped builder.' ) );
+
+		$builder_property = new ReflectionProperty( WP_AI_Client_Prompt_Builder::class, 'builder' );
+		self::set_accessible( $builder_property );
+		$builder_property->setValue( $prompt_builder, $wrapped_builder );
+
+		$result = $prompt_builder->{$method}();
+
+		$this->assertIsBool( $result, $method . ' should return a boolean' );
+		$this->assertFalse( $result, $method . ' should return false when the wrapped builder throws' );
+
+		// The error is still recorded, so a generating method returns it.
+		$error = $prompt_builder->generate_text();
+		$this->assertWPError( $error, 'The caught error should still be returned by generating methods' );
+		$this->assertSame(
+			'prompt_builder_error',
+			$error->get_error_code(),
+			'The recorded error should be the one thrown by the wrapped builder'
+		);
+	}
+
+	/**
+	 * Data provider.
+	 *
+	 * @return array<string, array{0: string, 1: string}> Support check method names, keyed by the method on the wrapper.
+	 */
+	public static function data_support_check_methods(): array {
+		return array(
+			'is_supported'                               => array( 'is_supported', 'isSupported' ),
+			'is_supported_for_text_generation'           => array( 'is_supported_for_text_generation', 'isSupportedForTextGeneration' ),
+			'is_supported_for_image_generation'          => array( 'is_supported_for_image_generation', 'isSupportedForImageGeneration' ),
+			'is_supported_for_text_to_speech_conversion' => array( 'is_supported_for_text_to_speech_conversion', 'isSupportedForTextToSpeechConversion' ),
+			'is_supported_for_video_generation'          => array( 'is_supported_for_video_generation', 'isSupportedForVideoGeneration' ),
+			'is_supported_for_speech_generation'         => array( 'is_supported_for_speech_generation', 'isSupportedForSpeechGeneration' ),
+			'is_supported_for_music_generation'          => array( 'is_supported_for_music_generation', 'isSupportedForMusicGeneration' ),
+			'is_supported_for_embedding_generation'      => array( 'is_supported_for_embedding_generation', 'isSupportedForEmbeddingGeneration' ),
+		);
+	}
+
+	/**
+	 * Tests that a throw from the bundled client during a support check is handled.
+	 *
+	 * This covers the route reported on the ticket. The document modality has no
+	 * capability to infer, so the wrapped builder throws while determining whether
+	 * the prompt is supported.
+	 *
+	 * @ticket 65781
+	 */
+	public function test_is_supported_returns_false_when_the_bundled_builder_throws() {
+		$registry       = AiClient::defaultRegistry();
+		$prompt_builder = new WP_AI_Client_Prompt_Builder( $registry, 'Test text' );
+
+		$result = $prompt_builder->as_output_modalities( ModalityEnum::document() )->is_supported();
+
+		$this->assertIsBool( $result, 'is_supported should return a boolean' );
+		$this->assertFalse( $result, 'is_supported should return false when the wrapped builder throws' );
+
+		$error = $prompt_builder->generate_text();
+		$this->assertWPError( $error, 'The caught error should still be returned by generating methods' );
+		$this->assertSame(
+			'prompt_builder_error',
+			$error->get_error_code(),
+			'The document modality should still throw from the wrapped builder. If it no longer does, this test needs another route to a throw'
+		);
+	}
+
 	/**
 	 * Tests that generating methods return WP_Error when in error state.
 	 *