diff --git a/docs/sample_config.yaml b/docs/sample_config.yaml
index 0c6be30e5..c96eb0cf2 100644
--- a/docs/sample_config.yaml
+++ b/docs/sample_config.yaml
@@ -1027,6 +1027,14 @@ signing_key_path: "CONFDIR/SERVERNAME.signing.key"
 #
 #trusted_key_servers:
 #  - server_name: "matrix.org"
+#
+
+# The additional signing keys to use when acting as a trusted key server, on
+# top of the normal signing keys.
+#
+# Can contain multiple keys, one per line.
+#
+#key_server_signing_keys_path: "key_server_signing_keys.key"
 
 
 # Enable SAML2 for registration and login. Uses pysaml2.
diff --git a/synapse/config/key.py b/synapse/config/key.py
index fe8386985..f1a1efcb7 100644
--- a/synapse/config/key.py
+++ b/synapse/config/key.py
@@ -76,7 +76,7 @@ class KeyConfig(Config):
                     config_dir_path, config["server_name"] + ".signing.key"
                 )
 
-            self.signing_key = self.read_signing_key(signing_key_path)
+            self.signing_key = self.read_signing_keys(signing_key_path, "signing_key")
 
         self.old_signing_keys = self.read_old_signing_keys(
             config.get("old_signing_keys", {})
@@ -85,6 +85,15 @@ class KeyConfig(Config):
             config.get("key_refresh_interval", "1d")
         )
 
+        self.key_server_signing_keys = list(self.signing_key)
+        key_server_signing_keys_path = config.get("key_server_signing_keys_path")
+        if key_server_signing_keys_path:
+            self.key_server_signing_keys.extend(
+                self.read_signing_keys(
+                    key_server_signing_keys_path, "key_server_signing_keys_path"
+                )
+            )
+
         # if neither trusted_key_servers nor perspectives are given, use the default.
         if "perspectives" not in config and "trusted_key_servers" not in config:
             key_servers = [{"server_name": "matrix.org"}]
@@ -210,16 +219,34 @@ class KeyConfig(Config):
         #
         #trusted_key_servers:
         #  - server_name: "matrix.org"
+        #
+
+        # The additional signing keys to use when acting as a trusted key server, on
+        # top of the normal signing keys.
+        #
+        # Can contain multiple keys, one per line.
+        #
+        #key_server_signing_keys_path: "key_server_signing_keys.key"
         """
             % locals()
         )
 
-    def read_signing_key(self, signing_key_path):
-        signing_keys = self.read_file(signing_key_path, "signing_key")
+    def read_signing_keys(self, signing_key_path, name):
+        """Read the signing keys in the given path.
+
+        Args:
+            signing_key_path (str)
+            name (str): Associated config key name
+
+        Returns:
+            list[SigningKey]
+        """
+
+        signing_keys = self.read_file(signing_key_path, name)
         try:
             return read_signing_keys(signing_keys.splitlines(True))
         except Exception as e:
-            raise ConfigError("Error reading signing_key: %s" % (str(e)))
+            raise ConfigError("Error reading %s: %s" % (name, str(e)))
 
     def read_old_signing_keys(self, old_signing_keys):
         keys = {}
diff --git a/synapse/crypto/keyring.py b/synapse/crypto/keyring.py
index 6c3e885e7..a3b55e349 100644
--- a/synapse/crypto/keyring.py
+++ b/synapse/crypto/keyring.py
@@ -540,11 +540,13 @@ class BaseV2KeyFetcher(object):
                     verify_key=verify_key, valid_until_ts=key_data["expired_ts"]
                 )
 
-        # re-sign the json with our own key, so that it is ready if we are asked to
-        # give it out as a notary server
-        signed_key_json = sign_json(
-            response_json, self.config.server_name, self.config.signing_key[0]
-        )
+        # re-sign the json with our own keys, so that it is ready if we are
+        # asked to give it out as a notary server
+        signed_key_json = response_json
+        for signing_key in self.config.key_server_signing_keys:
+            signed_key_json = sign_json(
+                signed_key_json, self.config.server_name, signing_key
+            )
 
         signed_key_json_bytes = encode_canonical_json(signed_key_json)