diff --git a/src/wp-includes/rest-api/class-wp-rest-request.php b/src/wp-includes/rest-api/class-wp-rest-request.php
index 73548d4f38..937b5684cd 100644
--- a/src/wp-includes/rest-api/class-wp-rest-request.php
+++ b/src/wp-includes/rest-api/class-wp-rest-request.php
@@ -858,13 +858,9 @@ class WP_REST_Request implements ArrayAccess {
 		$attributes = $this->get_attributes();
 		$required   = array();
 
-		// No arguments set, skip validation.
-		if ( empty( $attributes['args'] ) ) {
-			return true;
-		}
-
-		foreach ( $attributes['args'] as $key => $arg ) {
+		$args = empty( $attributes['args'] ) ? array() : $attributes['args'];
 
+		foreach ( $args as $key => $arg ) {
 			$param = $this->get_param( $key );
 			if ( isset( $arg['required'] ) && true === $arg['required'] && null === $param ) {
 				$required[] = $key;
@@ -890,7 +886,7 @@ class WP_REST_Request implements ArrayAccess {
 		 */
 		$invalid_params = array();
 
-		foreach ( $attributes['args'] as $key => $arg ) {
+		foreach ( $args as $key => $arg ) {
 
 			$param = $this->get_param( $key );
 
@@ -919,8 +915,20 @@ class WP_REST_Request implements ArrayAccess {
 			);
 		}
 
-		return true;
+		if ( isset( $attributes['validate_callback'] ) ) {
+			$valid_check = call_user_func( $attributes['validate_callback'], $this );
 
+			if ( is_wp_error( $valid_check ) ) {
+				return $valid_check;
+			}
+
+			if ( false === $valid_check ) {
+				// A WP_Error instance is preferred, but false is supported for parity with the per-arg validate_callback.
+				return new WP_Error( 'rest_invalid_params', __( 'Invalid parameters.' ), array( 'status' => 400 ) );
+			}
+		}
+
+		return true;
 	}
 
 	/**
diff --git a/tests/phpunit/tests/rest-api/rest-request.php b/tests/phpunit/tests/rest-api/rest-request.php
index 7ad78d81aa..d2f5021ce2 100644
--- a/tests/phpunit/tests/rest-api/rest-request.php
+++ b/tests/phpunit/tests/rest-api/rest-request.php
@@ -779,4 +779,72 @@ class Tests_REST_Request extends WP_UnitTestCase {
 		$this->assertTrue( $request->has_param( 'param' ) );
 		$this->assertSame( 'value', $request->get_param( 'param' ) );
 	}
+
+	/**
+	 * @ticket 51255
+	 */
+	public function test_route_level_validate_callback() {
+		$request = new WP_REST_Request();
+		$request->set_query_params( array( 'test' => 'value' ) );
+
+		$error    = new WP_Error( 'error_code', __( 'Error Message' ), array( 'status' => 400 ) );
+		$callback = $this->createPartialMock( 'stdClass', array( '__invoke' ) );
+		$callback->expects( self::once() )->method( '__invoke' )->with( self::identicalTo( $request ) )->willReturn( $error );
+		$request->set_attributes(
+			array(
+				'args'              => array(
+					'test' => array(
+						'validate_callback' => '__return_true',
+					),
+				),
+				'validate_callback' => $callback,
+			)
+		);
+
+		$this->assertSame( $error, $request->has_valid_params() );
+	}
+
+	/**
+	 * @ticket 51255
+	 */
+	public function test_route_level_validate_callback_no_parameter_callbacks() {
+		$request = new WP_REST_Request();
+		$request->set_query_params( array( 'test' => 'value' ) );
+
+		$error    = new WP_Error( 'error_code', __( 'Error Message' ), array( 'status' => 400 ) );
+		$callback = $this->createPartialMock( 'stdClass', array( '__invoke' ) );
+		$callback->expects( self::once() )->method( '__invoke' )->with( self::identicalTo( $request ) )->willReturn( $error );
+		$request->set_attributes(
+			array(
+				'validate_callback' => $callback,
+			)
+		);
+
+		$this->assertSame( $error, $request->has_valid_params() );
+	}
+
+	/**
+	 * @ticket 51255
+	 */
+	public function test_route_level_validate_callback_is_not_executed_if_parameter_validation_fails() {
+		$request = new WP_REST_Request();
+		$request->set_query_params( array( 'test' => 'value' ) );
+
+		$callback = $this->createPartialMock( 'stdClass', array( '__invoke' ) );
+		$callback->expects( self::never() )->method( '__invoke' );
+		$request->set_attributes(
+			array(
+				'validate_callback' => $callback,
+				'args'              => array(
+					'test' => array(
+						'validate_callback' => '__return_false',
+					),
+				),
+			)
+		);
+
+		$valid = $request->has_valid_params();
+		$this->assertWPError( $valid );
+		$this->assertEquals( 'rest_invalid_param', $valid->get_error_code() );
+	}
 }