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..8e2c04ba05be3 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
@@ -364,6 +364,9 @@ 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..bfec952718396 100644
--- a/tests/phpunit/tests/ai-client/wpAiClientPromptBuilder.php
+++ b/tests/phpunit/tests/ai-client/wpAiClientPromptBuilder.php
@@ -2648,6 +2648,28 @@ 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
+	 */
+	public function test_support_check_methods_return_false_when_builder_throws() {
+		$registry       = AiClient::defaultRegistry();
+		$prompt_builder = new WP_AI_Client_Prompt_Builder( $registry, 'Test text' );
+
+		/*
+		 * The document modality has no capability to infer, so the wrapped builder
+		 * throws while determining whether the prompt is supported.
+		 */
+		$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' );
+
+		// The error is still recorded, so a generating method returns it.
+		$this->assertWPError( $prompt_builder->generate_text(), 'The caught error should still be returned by generating methods' );
+	}
+
 	/**
 	 * Tests that generating methods return WP_Error when in error state.
 	 *