diff --git a/docs/brief-install-vagrant-dev.md b/docs/brief-install-vagrant-dev.md
index 7d2025c720..fc7ab0f3e8 100644
--- a/docs/brief-install-vagrant-dev.md
+++ b/docs/brief-install-vagrant-dev.md
@@ -62,18 +62,12 @@ Once that finishes, you can run the development server as follows:
 ```
 vagrant ssh
 # Now inside the container
-/srv/zulip/tools/run-dev.py --interface=''
+/srv/zulip/tools/run-dev.py
 ```
 
 To get shell access to the virtual machine running the server to run
 lint, management commands, etc., use `vagrant ssh`.
 
-(A small note on tools/run-dev.py: the `--interface=''` option will
-make the development server listen on all network interfaces.  While
-this is correct for the Vagrant guest sitting behind a NAT, you
-probably don't want to use that option when using run-dev.py in other
-environments).
-
 At this point you should [read about using the development
 environment][using-dev].
 
diff --git a/docs/dev-env-first-time-contributors.md b/docs/dev-env-first-time-contributors.md
index f52df5421a..2ba7e443e4 100644
--- a/docs/dev-env-first-time-contributors.md
+++ b/docs/dev-env-first-time-contributors.md
@@ -300,7 +300,7 @@ Next, start the Zulip server:
 
 ```
 (zulip-venv)vagrant@vagrant-ubuntu-trusty-64:~ $
-/srv/zulip/tools/run-dev.py --interface=''
+/srv/zulip/tools/run-dev.py
 ```
 
 As you can see above the application's root directory, where you can
@@ -477,7 +477,7 @@ server:
 christie@win10 ~/zulip
 $ vagrant up
 $ vagrant ssh
-/srv/zulip/tools/run-dev.py --interface=''
+/srv/zulip/tools/run-dev.py
 ```
 
 #### Next Steps
diff --git a/tools/run-dev.py b/tools/run-dev.py
index d9b313020f..5f2e99cf6b 100755
--- a/tools/run-dev.py
+++ b/tools/run-dev.py
@@ -2,6 +2,7 @@
 from __future__ import print_function
 
 import optparse
+import pwd
 import subprocess
 import signal
 import traceback
@@ -57,7 +58,7 @@ parser.add_option('--test',
 
 parser.add_option('--interface',
     action='store', dest='interface',
-    default='127.0.0.1', help='Set the IP or hostname for the proxy to listen on')
+    default=None, help='Set the IP or hostname for the proxy to listen on')
 
 parser.add_option('--no-clear-memcached',
     action='store_false', dest='clear_memcached',
@@ -65,6 +66,18 @@ parser.add_option('--no-clear-memcached',
 
 (options, args) = parser.parse_args()
 
+if options.interface is None:
+    user_id = os.getuid()
+    user_name = pwd.getpwuid(user_id).pw_name
+    if user_name == "vagrant":
+        # In the Vagrant development environment, we need to listen on
+        # all ports, and it's safe to do so, because Vagrant is only
+        # exposing certain guest ports (by default just 9991) to the host.
+        options.interface = ""
+    else:
+        # Otherwise, only listen to requests on localhost for security.
+        options.interface = "127.0.0.1"
+
 base_port   = 9991
 if options.test:
     base_port   = 9981