diff --git a/synapse/app/appservice.py b/synapse/app/appservice.py
index c1379fdd7..190093005 100644
--- a/synapse/app/appservice.py
+++ b/synapse/app/appservice.py
@@ -76,8 +76,7 @@ class AppserviceServer(HomeServer):
 
     def _listen_http(self, listener_config):
         port = listener_config["port"]
-        bind_address = listener_config.get("bind_address", None)
-        bind_addresses = listener_config.get("bind_addresses", [])
+        bind_addresses = listener_config["bind_addresses"]
         site_tag = listener_config.get("tag", port)
         resources = {}
         for res in listener_config["resources"]:
@@ -87,9 +86,6 @@ class AppserviceServer(HomeServer):
 
         root_resource = create_resource_tree(resources, Resource())
 
-        if bind_address is not None:
-            bind_addresses.append(bind_address)
-
         for address in bind_addresses:
             reactor.listenTCP(
                 port,
@@ -109,11 +105,7 @@ class AppserviceServer(HomeServer):
             if listener["type"] == "http":
                 self._listen_http(listener)
             elif listener["type"] == "manhole":
-                bind_address = listener.get("bind_address", None)
-                bind_addresses = listener.get("bind_addresses", [])
-
-                if bind_address is not None:
-                    bind_addresses.append(bind_address)
+                bind_addresses = listener["bind_addresses"]
 
                 for address in bind_addresses:
                     reactor.listenTCP(
diff --git a/synapse/app/client_reader.py b/synapse/app/client_reader.py
index b5e1d659e..4d081eccd 100644
--- a/synapse/app/client_reader.py
+++ b/synapse/app/client_reader.py
@@ -90,8 +90,7 @@ class ClientReaderServer(HomeServer):
 
     def _listen_http(self, listener_config):
         port = listener_config["port"]
-        bind_address = listener_config.get("bind_address", None)
-        bind_addresses = listener_config.get("bind_addresses", [])
+        bind_addresses = listener_config["bind_addresses"]
         site_tag = listener_config.get("tag", port)
         resources = {}
         for res in listener_config["resources"]:
@@ -110,9 +109,6 @@ class ClientReaderServer(HomeServer):
 
         root_resource = create_resource_tree(resources, Resource())
 
-        if bind_address is not None:
-            bind_addresses.append(bind_address)
-
         for address in bind_addresses:
             reactor.listenTCP(
                 port,
@@ -132,11 +128,7 @@ class ClientReaderServer(HomeServer):
             if listener["type"] == "http":
                 self._listen_http(listener)
             elif listener["type"] == "manhole":
-                bind_address = listener.get("bind_address", None)
-                bind_addresses = listener.get("bind_addresses", [])
-
-                if bind_address is not None:
-                    bind_addresses.append(bind_address)
+                bind_addresses = listener["bind_addresses"]
 
                 for address in bind_addresses:
                     reactor.listenTCP(
diff --git a/synapse/app/federation_reader.py b/synapse/app/federation_reader.py
index c6810b83d..90a481675 100644
--- a/synapse/app/federation_reader.py
+++ b/synapse/app/federation_reader.py
@@ -86,8 +86,7 @@ class FederationReaderServer(HomeServer):
 
     def _listen_http(self, listener_config):
         port = listener_config["port"]
-        bind_address = listener_config.get("bind_address", None)
-        bind_addresses = listener_config.get("bind_addresses", [])
+        bind_addresses = listener_config["bind_addresses"]
         site_tag = listener_config.get("tag", port)
         resources = {}
         for res in listener_config["resources"]:
@@ -101,9 +100,6 @@ class FederationReaderServer(HomeServer):
 
         root_resource = create_resource_tree(resources, Resource())
 
-        if bind_address is not None:
-            bind_addresses.append(bind_address)
-
         for address in bind_addresses:
             reactor.listenTCP(
                 port,
@@ -123,11 +119,7 @@ class FederationReaderServer(HomeServer):
             if listener["type"] == "http":
                 self._listen_http(listener)
             elif listener["type"] == "manhole":
-                bind_address = listener.get("bind_address", None)
-                bind_addresses = listener.get("bind_addresses", [])
-
-                if bind_address is not None:
-                    bind_addresses.append(bind_address)
+                bind_addresses = listener["bind_addresses"]
 
                 for address in bind_addresses:
                     reactor.listenTCP(
diff --git a/synapse/app/federation_sender.py b/synapse/app/federation_sender.py
index 23aae8a09..ec06620ef 100644
--- a/synapse/app/federation_sender.py
+++ b/synapse/app/federation_sender.py
@@ -82,8 +82,7 @@ class FederationSenderServer(HomeServer):
 
     def _listen_http(self, listener_config):
         port = listener_config["port"]
-        bind_address = listener_config.get("bind_address", None)
-        bind_addresses = listener_config.get("bind_addresses", [])
+        bind_addresses = listener_config["bind_addresses"]
         site_tag = listener_config.get("tag", port)
         resources = {}
         for res in listener_config["resources"]:
@@ -93,9 +92,6 @@ class FederationSenderServer(HomeServer):
 
         root_resource = create_resource_tree(resources, Resource())
 
-        if bind_address is not None:
-            bind_addresses.append(bind_address)
-
         for address in bind_addresses:
             reactor.listenTCP(
                 port,
@@ -115,11 +111,7 @@ class FederationSenderServer(HomeServer):
             if listener["type"] == "http":
                 self._listen_http(listener)
             elif listener["type"] == "manhole":
-                bind_address = listener.get("bind_address", None)
-                bind_addresses = listener.get("bind_addresses", [])
-
-                if bind_address is not None:
-                    bind_addresses.append(bind_address)
+                bind_addresses = listener["bind_addresses"]
 
                 for address in bind_addresses:
                     reactor.listenTCP(
diff --git a/synapse/app/homeserver.py b/synapse/app/homeserver.py
index 6c69ccd7e..e0b87468f 100755
--- a/synapse/app/homeserver.py
+++ b/synapse/app/homeserver.py
@@ -107,8 +107,7 @@ def build_resource_for_web_client(hs):
 class SynapseHomeServer(HomeServer):
     def _listener_http(self, config, listener_config):
         port = listener_config["port"]
-        bind_address = listener_config.get("bind_address", None)
-        bind_addresses = listener_config.get("bind_addresses", [])
+        bind_addresses = listener_config["bind_addresses"]
         tls = listener_config.get("tls", False)
         site_tag = listener_config.get("tag", port)
 
@@ -175,9 +174,6 @@ class SynapseHomeServer(HomeServer):
 
         root_resource = create_resource_tree(resources, root_resource)
 
-        if bind_address is not None:
-            bind_addresses.append(bind_address)
-
         if tls:
             for address in bind_addresses:
                 reactor.listenSSL(
@@ -212,11 +208,7 @@ class SynapseHomeServer(HomeServer):
             if listener["type"] == "http":
                 self._listener_http(config, listener)
             elif listener["type"] == "manhole":
-                bind_address = listener.get("bind_address", None)
-                bind_addresses = listener.get("bind_addresses", [])
-
-                if bind_address is not None:
-                    bind_addresses.append(bind_address)
+                bind_addresses = listener["bind_addresses"]
 
                 for address in bind_addresses:
                     reactor.listenTCP(
diff --git a/synapse/app/media_repository.py b/synapse/app/media_repository.py
index a47283e52..ef17b158a 100644
--- a/synapse/app/media_repository.py
+++ b/synapse/app/media_repository.py
@@ -87,8 +87,7 @@ class MediaRepositoryServer(HomeServer):
 
     def _listen_http(self, listener_config):
         port = listener_config["port"]
-        bind_address = listener_config.get("bind_address", None)
-        bind_addresses = listener_config.get("bind_addresses", [])
+        bind_addresses = listener_config["bind_addresses"]
         site_tag = listener_config.get("tag", port)
         resources = {}
         for res in listener_config["resources"]:
@@ -107,9 +106,6 @@ class MediaRepositoryServer(HomeServer):
 
         root_resource = create_resource_tree(resources, Resource())
 
-        if bind_address is not None:
-            bind_addresses.append(bind_address)
-
         for address in bind_addresses:
             reactor.listenTCP(
                 port,
@@ -129,11 +125,7 @@ class MediaRepositoryServer(HomeServer):
             if listener["type"] == "http":
                 self._listen_http(listener)
             elif listener["type"] == "manhole":
-                bind_address = listener.get("bind_address", None)
-                bind_addresses = listener.get("bind_addresses", [])
-
-                if bind_address is not None:
-                    bind_addresses.append(bind_address)
+                bind_addresses = listener["bind_addresses"]
 
                 for address in bind_addresses:
                     reactor.listenTCP(
diff --git a/synapse/app/pusher.py b/synapse/app/pusher.py
index 57e097fa1..073f2c248 100644
--- a/synapse/app/pusher.py
+++ b/synapse/app/pusher.py
@@ -121,8 +121,7 @@ class PusherServer(HomeServer):
 
     def _listen_http(self, listener_config):
         port = listener_config["port"]
-        bind_address = listener_config.get("bind_address", None)
-        bind_addresses = listener_config.get("bind_addresses", [])
+        bind_addresses = listener_config["bind_addresses"]
         site_tag = listener_config.get("tag", port)
         resources = {}
         for res in listener_config["resources"]:
@@ -132,9 +131,6 @@ class PusherServer(HomeServer):
 
         root_resource = create_resource_tree(resources, Resource())
 
-        if bind_address is not None:
-            bind_addresses.append(bind_address)
-
         for address in bind_addresses:
             reactor.listenTCP(
                 port,
@@ -154,11 +150,7 @@ class PusherServer(HomeServer):
             if listener["type"] == "http":
                 self._listen_http(listener)
             elif listener["type"] == "manhole":
-                bind_address = listener.get("bind_address", None)
-                bind_addresses = listener.get("bind_addresses", [])
-
-                if bind_address is not None:
-                    bind_addresses.append(bind_address)
+                bind_addresses = listener["bind_addresses"]
 
                 for address in bind_addresses:
                     reactor.listenTCP(
diff --git a/synapse/app/synchrotron.py b/synapse/app/synchrotron.py
index 439daaa60..4dfc2dc64 100644
--- a/synapse/app/synchrotron.py
+++ b/synapse/app/synchrotron.py
@@ -289,8 +289,7 @@ class SynchrotronServer(HomeServer):
 
     def _listen_http(self, listener_config):
         port = listener_config["port"]
-        bind_address = listener_config.get("bind_address", None)
-        bind_addresses = listener_config.get("bind_addresses", [])
+        bind_addresses = listener_config["bind_addresses"]
         site_tag = listener_config.get("tag", port)
         resources = {}
         for res in listener_config["resources"]:
@@ -312,9 +311,6 @@ class SynchrotronServer(HomeServer):
 
         root_resource = create_resource_tree(resources, Resource())
 
-        if bind_address is not None:
-            bind_addresses.append(bind_address)
-
         for address in bind_addresses:
             reactor.listenTCP(
                 port,
@@ -334,11 +330,7 @@ class SynchrotronServer(HomeServer):
             if listener["type"] == "http":
                 self._listen_http(listener)
             elif listener["type"] == "manhole":
-                bind_address = listener.get("bind_address", None)
-                bind_addresses = listener.get("bind_addresses", [])
-
-                if bind_address is not None:
-                    bind_addresses.append(bind_address)
+                bind_addresses = listener["bind_addresses"]
 
                 for address in bind_addresses:
                     reactor.listenTCP(
diff --git a/synapse/config/server.py b/synapse/config/server.py
index 5e6b2a68a..59687ee39 100644
--- a/synapse/config/server.py
+++ b/synapse/config/server.py
@@ -42,6 +42,15 @@ class ServerConfig(Config):
 
         self.listeners = config.get("listeners", [])
 
+        for listener in self.listeners:
+            bind_address = listener.get("bind_address", None)
+            bind_addresses = listener.setdefault("bind_addresses", [])
+
+            if bind_address:
+                bind_addresses.append(bind_address)
+            elif not bind_addresses:
+                bind_addresses.append('')
+
         self.gc_thresholds = read_gc_thresholds(config.get("gc_thresholds", None))
 
         bind_port = config.get("bind_port")
@@ -54,7 +63,7 @@ class ServerConfig(Config):
 
             self.listeners.append({
                 "port": bind_port,
-                "bind_address": bind_host,
+                "bind_addresses": [bind_host],
                 "tls": True,
                 "type": "http",
                 "resources": [
@@ -73,7 +82,7 @@ class ServerConfig(Config):
             if unsecure_port:
                 self.listeners.append({
                     "port": unsecure_port,
-                    "bind_address": bind_host,
+                    "bind_addresses": [bind_host],
                     "tls": False,
                     "type": "http",
                     "resources": [
@@ -92,7 +101,7 @@ class ServerConfig(Config):
         if manhole:
             self.listeners.append({
                 "port": manhole,
-                "bind_address": "127.0.0.1",
+                "bind_addresses": ["127.0.0.1"],
                 "type": "manhole",
             })
 
@@ -100,7 +109,7 @@ class ServerConfig(Config):
         if metrics_port:
             self.listeners.append({
                 "port": metrics_port,
-                "bind_address": config.get("metrics_bind_host", "127.0.0.1"),
+                "bind_addresses": [config.get("metrics_bind_host", "127.0.0.1")],
                 "tls": False,
                 "type": "http",
                 "resources": [