diff --git a/zerver/tests/test_integrations.py b/zerver/tests/test_integrations.py
index 039d27d106..9f779a2901 100644
--- a/zerver/tests/test_integrations.py
+++ b/zerver/tests/test_integrations.py
@@ -23,22 +23,22 @@ class IntegrationTest(TestCase):
         # type: () -> None
         context = dict()  # type: Dict[str, Any]
         add_api_uri_context(context, HostRequestMock())
-        self.assertEqual(context["external_api_path_subdomain"], "zulipdev.com:9991/api")
-        self.assertEqual(context["external_api_uri_subdomain"], "http://zulipdev.com:9991/api")
+        self.assertEqual(context["external_api_path_subdomain"], "testserver/api")
+        self.assertEqual(context["external_api_uri_subdomain"], "http://testserver/api")
 
     @override_settings(REALMS_HAVE_SUBDOMAINS=True)
     def test_api_url_view_subdomains_base(self):
         # type: () -> None
         context = dict()  # type: Dict[str, Any]
         add_api_uri_context(context, HostRequestMock())
-        self.assertEqual(context["external_api_path_subdomain"], "yourZulipDomain.zulipdev.com:9991/api")
-        self.assertEqual(context["external_api_uri_subdomain"], "http://yourZulipDomain.zulipdev.com:9991/api")
+        self.assertEqual(context["external_api_path_subdomain"], "yourZulipDomain.testserver/api")
+        self.assertEqual(context["external_api_uri_subdomain"], "http://yourZulipDomain.testserver/api")
 
-    @override_settings(REALMS_HAVE_SUBDOMAINS=True, EXTERNAL_HOST="zulipdev.com")
+    @override_settings(REALMS_HAVE_SUBDOMAINS=True)
     def test_api_url_view_subdomains_full(self):
         # type: () -> None
         context = dict()  # type: Dict[str, Any]
-        request = HostRequestMock(host="mysubdomain.zulipdev.com")
+        request = HostRequestMock(host="mysubdomain.testserver")
         add_api_uri_context(context, request)
-        self.assertEqual(context["external_api_path_subdomain"], "mysubdomain.zulipdev.com:9991/api")
-        self.assertEqual(context["external_api_uri_subdomain"], "http://mysubdomain.zulipdev.com:9991/api")
+        self.assertEqual(context["external_api_path_subdomain"], "mysubdomain.testserver/api")
+        self.assertEqual(context["external_api_uri_subdomain"], "http://mysubdomain.testserver/api")
diff --git a/zproject/dev_settings.py b/zproject/dev_settings.py
index ef047b3dcf..3cd5338238 100644
--- a/zproject/dev_settings.py
+++ b/zproject/dev_settings.py
@@ -2,9 +2,12 @@
 # For the Dev VM environment, we use the same settings as the
 # sample prod_settings.py file, with a few exceptions.
 from .prod_settings_template import *
+import os
 
 LOCAL_UPLOADS_DIR = 'var/uploads'
-EXTERNAL_HOST = 'zulipdev.com:9991'
+# We check the environment to support test_settings.py controlling
+# EXTERNAL_HOST.
+EXTERNAL_HOST = os.getenv('EXTERNAL_HOST', 'zulipdev.com:9991')
 ALLOWED_HOSTS = ['*']
 AUTHENTICATION_BACKENDS = ('zproject.backends.DevAuthBackend',)
 # Add some of the below if you're testing other backends
diff --git a/zproject/test_settings.py b/zproject/test_settings.py
index 340bb6c0c9..d717fa869e 100644
--- a/zproject/test_settings.py
+++ b/zproject/test_settings.py
@@ -1,6 +1,23 @@
 from __future__ import absolute_import
-from .settings import *
 import os
+# test_settings.py works differently from
+# dev_settings.py/prod_settings.py; it actually is directly referenced
+# by the test suite as DJANGO_SETTINGS_MODULE and imports settings.py
+# directly and then hacks up the values that are different for the
+# test suite.  As will be explained, this is kinda messy and probably
+# we'd be better off switching it to work more like dev_settings.py,
+# but for now, this is what we have.
+#
+# An important downside of the test_settings.py approach is that if we
+# want to change any settings that settings.py then computes
+# additional settings from (e.g. EXTERNAL_HOST), we need to do a hack
+# like the below line(s) before we import from settings, for
+# transmitting the value of EXTERNAL_HOST to dev_settings.py so that
+# it can be set there, at the right place in the settings.py flow.
+# Ick.
+if os.getenv("EXTERNAL_HOST") is None:
+    os.environ["EXTERNAL_HOST"] = "testserver"
+from .settings import *
 
 DATABASES["default"] = {"NAME": "zulip_test",
                         "USER": "zulip_test",
@@ -82,7 +99,6 @@ LOCAL_UPLOADS_DIR = 'var/test_uploads'
 S3_KEY = 'test-key'
 S3_SECRET_KEY = 'test-secret-key'
 S3_AUTH_UPLOADS_BUCKET = 'test-authed-bucket'
-EXTERNAL_HOST = os.getenv('EXTERNAL_HOST', "testserver")
 REALMS_HAVE_SUBDOMAINS = bool(os.getenv('REALMS_HAVE_SUBDOMAINS', False))
 
 # Test Custom TOS template rendering