diff --git a/rest_framework/views.py b/rest_framework/views.py
index 6ef7021d4..832f17233 100644
--- a/rest_framework/views.py
+++ b/rest_framework/views.py
@@ -350,9 +350,13 @@ class APIView(View):
         Check if request should be throttled.
         Raises an appropriate exception if the request is throttled.
         """
+        throttle_durations = []
         for throttle in self.get_throttles():
             if not throttle.allow_request(request, self):
-                self.throttled(request, throttle.wait())
+                throttle_durations.append(throttle.wait())
+
+        if throttle_durations:
+            self.throttled(request, max(throttle_durations))
 
     def determine_version(self, request, *args, **kwargs):
         """
diff --git a/tests/test_throttling.py b/tests/test_throttling.py
index b20b6a809..3c172e263 100644
--- a/tests/test_throttling.py
+++ b/tests/test_throttling.py
@@ -30,6 +30,11 @@ class User3MinRateThrottle(UserRateThrottle):
     scope = 'minutes'
 
 
+class User6MinRateThrottle(UserRateThrottle):
+    rate = '6/min'
+    scope = 'minutes'
+
+
 class NonTimeThrottle(BaseThrottle):
     def allow_request(self, request, view):
         if not hasattr(self.__class__, 'called'):
@@ -38,6 +43,13 @@ class NonTimeThrottle(BaseThrottle):
         return False
 
 
+class MockView_DoubleThrottling(APIView):
+    throttle_classes = (User3SecRateThrottle, User6MinRateThrottle,)
+
+    def get(self, request):
+        return Response('foo')
+
+
 class MockView(APIView):
     throttle_classes = (User3SecRateThrottle,)
 
@@ -80,7 +92,8 @@ class ThrottlingTests(TestCase):
         """
         Explicitly set the timer, overriding time.time()
         """
-        view.throttle_classes[0].timer = lambda self: value
+        for cls in view.throttle_classes:
+            cls.timer = lambda self: value
 
     def test_request_throttling_expires(self):
         """
@@ -115,6 +128,37 @@ class ThrottlingTests(TestCase):
         """
         self.ensure_is_throttled(MockView, 200)
 
+    def test_request_throttling_multiple_throttles(self):
+        """
+        Ensure all throttle classes see each request even when the request is
+        already being throttled
+        """
+        self.set_throttle_timer(MockView_DoubleThrottling, 0)
+        request = self.factory.get('/')
+        for dummy in range(4):
+            response = MockView_DoubleThrottling.as_view()(request)
+        assert response.status_code == 429
+        assert int(response['retry-after']) == 1
+
+        # At this point our client made 4 requests (one was throttled) in a
+        # second. If we advance the timer by one additional second, the client
+        # should be allowed to make 2 more before being throttled by the 2nd
+        # throttle class, which has a limit of 6 per minute.
+        self.set_throttle_timer(MockView_DoubleThrottling, 1)
+        for dummy in range(2):
+            response = MockView_DoubleThrottling.as_view()(request)
+            assert response.status_code == 200
+
+        response = MockView_DoubleThrottling.as_view()(request)
+        assert response.status_code == 429
+        assert int(response['retry-after']) == 59
+
+        # Just to make sure check again after two more seconds.
+        self.set_throttle_timer(MockView_DoubleThrottling, 2)
+        response = MockView_DoubleThrottling.as_view()(request)
+        assert response.status_code == 429
+        assert int(response['retry-after']) == 58
+
     def ensure_response_header_contains_proper_throttle_field(self, view, expected_headers):
         """
         Ensure the response returns an Retry-After field with status and next attributes