diff --git a/chalice/app.py b/chalice/app.py
index 4fe176bf0..8f1e6f188 100644
--- a/chalice/app.py
+++ b/chalice/app.py
@@ -226,6 +226,7 @@ def __repr__(self) -> str:
 class Authorizer(object):
     name: str = ''
     scopes: List[str] = []
+    config: Optional['BuiltinAuthConfig'] = None
 
     def to_swagger(self) -> Dict[str, Any]:
         raise NotImplementedError("to_swagger")
diff --git a/chalice/local.py b/chalice/local.py
index 0c13f31ac..0dd0961ab 100644
--- a/chalice/local.py
+++ b/chalice/local.py
@@ -312,6 +312,10 @@ def authorize(self,
         authorizer = route_entry.authorizer
         if not authorizer:
             return lambda_event, lambda_context
+
+        auth_header = authorizer.config.header.lower()\
+            if authorizer.config else "authorization"
+
         # If authorizer is Cognito then try to parse the JWT and simulate an
         # APIGateway validated request
         if isinstance(authorizer, CognitoUserPoolAuthorizer):
@@ -353,8 +357,10 @@ def authorize(self,
             )
             return lambda_event, lambda_context
         arn = self._arn_builder.build_arn(method, raw_path)
-        auth_event = self._prepare_authorizer_event(arn, lambda_event,
-                                                    lambda_context)
+        auth_event = self._prepare_authorizer_event(arn,
+                                                    lambda_event,
+                                                    lambda_context,
+                                                    auth_header)
         auth_result = authorizer(auth_event, lambda_context)
         if auth_result is None:
             raise InvalidAuthorizerError(
@@ -417,13 +423,14 @@ def _update_lambda_event(self, lambda_event: EventType,
 
     def _prepare_authorizer_event(self, arn: str,
                                   lambda_event: EventType,
-                                  lambda_context: LambdaContext) -> EventType:
+                                  lambda_context: LambdaContext,
+                                  auth_header: str = 'authorization') -> EventType:
         """Translate event for an authorizer input."""
         authorizer_event = lambda_event.copy()
         authorizer_event['type'] = 'TOKEN'
         try:
             authorizer_event['authorizationToken'] = authorizer_event.get(
-                'headers', {})['authorization']
+                'headers', {})[auth_header]
         except KeyError:
             raise NotAuthorizedError(
                 {'x-amzn-RequestId': lambda_context.aws_request_id,