diff --git a/zerver/decorator.py b/zerver/decorator.py
index c2f7aaa940..4dc97f9243 100644
--- a/zerver/decorator.py
+++ b/zerver/decorator.py
@@ -22,13 +22,12 @@ from zerver.lib.queue import queue_json_publish
 from zerver.lib.subdomains import get_subdomain, user_matches_subdomain
 from zerver.lib.timestamp import datetime_to_timestamp, timestamp_to_datetime
 from zerver.lib.utils import statsd, is_remote_server
-from zerver.lib.exceptions import RateLimited, JsonableError, ErrorCode, \
+from zerver.lib.exceptions import JsonableError, ErrorCode, \
     InvalidJSONError, InvalidAPIKeyError
 from zerver.lib.types import ViewFuncT
 from zerver.lib.validator import to_non_negative_int
 
-from zerver.lib.rate_limiter import rate_limit_entity, \
-    api_calls_left, RateLimitedUser
+from zerver.lib.rate_limiter import rate_limit_request_by_entity, RateLimitedUser
 from zerver.lib.request import REQ, has_request_variables
 
 from functools import wraps
@@ -746,18 +745,7 @@ def rate_limit_user(request: HttpRequest, user: UserProfile, domain: str) -> Non
     the rate limit information"""
 
     entity = RateLimitedUser(user, domain=domain)
-    ratelimited, time = rate_limit_entity(entity)
-    request._ratelimit_applied_limits = True
-    request._ratelimit_secs_to_freedom = time
-    request._ratelimit_over_limit = ratelimited
-    # Abort this request if the user is over their rate limits
-    if ratelimited:
-        raise RateLimited()
-
-    calls_remaining, time_reset = api_calls_left(entity)
-
-    request._ratelimit_remaining = calls_remaining
-    request._ratelimit_secs_to_freedom = time_reset
+    rate_limit_request_by_entity(request, entity)
 
 def rate_limit(domain: str='all') -> Callable[[ViewFuncT], ViewFuncT]:
     """Rate-limits a view. Takes an optional 'domain' param if you wish to
diff --git a/zerver/lib/rate_limiter.py b/zerver/lib/rate_limiter.py
index 134d0ef4ca..32bfe73646 100644
--- a/zerver/lib/rate_limiter.py
+++ b/zerver/lib/rate_limiter.py
@@ -4,6 +4,8 @@ import os
 from typing import List, Optional, Tuple
 
 from django.conf import settings
+from django.http import HttpRequest
+from zerver.lib.exceptions import RateLimited
 from zerver.lib.redis_utils import get_redis_client
 from zerver.lib.utils import statsd
 
@@ -261,3 +263,23 @@ def rate_limit_entity(entity: RateLimitedObject) -> Tuple[bool, float]:
             ratelimited = True
 
     return ratelimited, time
+
+def rate_limit_request_by_entity(request: HttpRequest, entity: RateLimitedObject) -> None:
+    ratelimited, time = rate_limit_entity(entity)
+
+    entity_type = type(entity).__name__
+    if not hasattr(request, '_ratelimit'):
+        request._ratelimit = {}
+    request._ratelimit[entity_type] = {}
+    request._ratelimit[entity_type]['applied_limits'] = True
+    request._ratelimit[entity_type]['secs_to_freedom'] = time
+    request._ratelimit[entity_type]['over_limit'] = ratelimited
+    # Abort this request if the user is over their rate limits
+    if ratelimited:
+        # Pass information about what kind of entity got limited in the exception:
+        raise RateLimited(entity_type)
+
+    calls_remaining, time_reset = api_calls_left(entity)
+
+    request._ratelimit[entity_type]['remaining'] = calls_remaining
+    request._ratelimit[entity_type]['secs_to_freedom'] = time_reset
diff --git a/zerver/middleware.py b/zerver/middleware.py
index 3eb1de29f3..8dfe0fe4eb 100644
--- a/zerver/middleware.py
+++ b/zerver/middleware.py
@@ -326,23 +326,25 @@ class RateLimitMiddleware(MiddlewareMixin):
 
         from zerver.lib.rate_limiter import max_api_calls, RateLimitedUser
         # Add X-RateLimit-*** headers
-        if hasattr(request, '_ratelimit_applied_limits'):
+        if hasattr(request, '_ratelimit'):
+            # Right now, the only kind of limiting requests is user-based.
+            ratelimit_user_results = request._ratelimit['RateLimitedUser']
             entity = RateLimitedUser(request.user)
             response['X-RateLimit-Limit'] = str(max_api_calls(entity))
-            if hasattr(request, '_ratelimit_secs_to_freedom'):
-                response['X-RateLimit-Reset'] = str(int(time.time() + request._ratelimit_secs_to_freedom))
-            if hasattr(request, '_ratelimit_remaining'):
-                response['X-RateLimit-Remaining'] = str(request._ratelimit_remaining)
+            response['X-RateLimit-Reset'] = str(int(time.time() + ratelimit_user_results['secs_to_freedom']))
+            if 'remaining' in ratelimit_user_results:
+                response['X-RateLimit-Remaining'] = str(ratelimit_user_results['remaining'])
         return response
 
     def process_exception(self, request: HttpRequest, exception: Exception) -> Optional[HttpResponse]:
         if isinstance(exception, RateLimited):
+            entity_type = str(exception)  # entity type is passed to RateLimited when raising
             resp = json_error(
                 _("API usage exceeded rate limit"),
-                data={'retry-after': request._ratelimit_secs_to_freedom},
+                data={'retry-after': request._ratelimit[entity_type]['secs_to_freedom']},
                 status=429
             )
-            resp['Retry-After'] = request._ratelimit_secs_to_freedom
+            resp['Retry-After'] = request._ratelimit[entity_type]['secs_to_freedom']
             return resp
         return None