diff --git a/changelog.d/16137.feature b/changelog.d/16137.feature
new file mode 100644
index 0000000000..bba6f161cd
--- /dev/null
+++ b/changelog.d/16137.feature
@@ -0,0 +1 @@
+Support resolving homeservers using `matrix-fed` DNS SRV records from [MSC4040](https://github.com/matrix-org/matrix-spec-proposals/pull/4040).
diff --git a/scripts-dev/federation_client.py b/scripts-dev/federation_client.py
index 5ad334b4d8..e8baeac5e2 100755
--- a/scripts-dev/federation_client.py
+++ b/scripts-dev/federation_client.py
@@ -329,6 +329,17 @@ class MatrixConnectionAdapter(HTTPAdapter):
                 raise ValueError("Invalid host:port '%s'" % (server_name,))
             return out[0], port, out[0]
 
+        # Look up SRV for Matrix 1.8 `matrix-fed` service first
+        try:
+            srv = srvlookup.lookup("matrix-fed", "tcp", server_name)[0]
+            print(
+                f"SRV lookup on _matrix-fed._tcp.{server_name} gave {srv}",
+                file=sys.stderr,
+            )
+            return srv.host, srv.port, server_name
+        except Exception:
+            pass
+        # Fall back to deprecated `matrix` service
         try:
             srv = srvlookup.lookup("matrix", "tcp", server_name)[0]
             print(
@@ -337,6 +348,7 @@ class MatrixConnectionAdapter(HTTPAdapter):
             )
             return srv.host, srv.port, server_name
         except Exception:
+            # Fall even further back to just port 8448
             return server_name, 8448, server_name
 
     @staticmethod
diff --git a/synapse/http/federation/matrix_federation_agent.py b/synapse/http/federation/matrix_federation_agent.py
index 91a24efcd0..a3a396bb37 100644
--- a/synapse/http/federation/matrix_federation_agent.py
+++ b/synapse/http/federation/matrix_federation_agent.py
@@ -399,15 +399,34 @@ class MatrixHostnameEndpoint:
         if port or _is_ip_literal(host):
             return [Server(host, port or 8448)]
 
+        # Check _matrix-fed._tcp SRV record.
         logger.debug("Looking up SRV record for %s", host.decode(errors="replace"))
+        server_list = await self._srv_resolver.resolve_service(
+            b"_matrix-fed._tcp." + host
+        )
+
+        if server_list:
+            if logger.isEnabledFor(logging.DEBUG):
+                logger.debug(
+                    "Got %s from SRV lookup for %s",
+                    ", ".join(map(str, server_list)),
+                    host.decode(errors="replace"),
+                )
+            return server_list
+
+        # No _matrix-fed._tcp SRV record, fallback to legacy _matrix._tcp SRV record.
+        logger.debug(
+            "Looking up deprecated SRV record for %s", host.decode(errors="replace")
+        )
         server_list = await self._srv_resolver.resolve_service(b"_matrix._tcp." + host)
 
         if server_list:
-            logger.debug(
-                "Got %s from SRV lookup for %s",
-                ", ".join(map(str, server_list)),
-                host.decode(errors="replace"),
-            )
+            if logger.isEnabledFor(logging.DEBUG):
+                logger.debug(
+                    "Got %s from deprecated SRV lookup for %s",
+                    ", ".join(map(str, server_list)),
+                    host.decode(errors="replace"),
+                )
             return server_list
 
         # No SRV records, so we fallback to host and 8448
diff --git a/tests/http/federation/test_matrix_federation_agent.py b/tests/http/federation/test_matrix_federation_agent.py
index 0d17f2fe5b..9f63fa6fa8 100644
--- a/tests/http/federation/test_matrix_federation_agent.py
+++ b/tests/http/federation/test_matrix_federation_agent.py
@@ -15,7 +15,7 @@ import base64
 import logging
 import os
 from typing import Generator, List, Optional, cast
-from unittest.mock import AsyncMock, patch
+from unittest.mock import AsyncMock, call, patch
 
 import treq
 from netaddr import IPSet
@@ -651,9 +651,9 @@ class MatrixFederationAgentTests(unittest.TestCase):
         # .well-known request fails.
         self.reactor.pump((0.4,))
 
-        # now there should be a SRV lookup
-        self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.testserv1"
+        # now there should be two SRV lookups
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [call(b"_matrix-fed._tcp.testserv1"), call(b"_matrix._tcp.testserv1")]
         )
 
         # we should fall back to a direct connection
@@ -737,9 +737,9 @@ class MatrixFederationAgentTests(unittest.TestCase):
         # .well-known request fails.
         self.reactor.pump((0.4,))
 
-        # now there should be a SRV lookup
-        self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.testserv"
+        # now there should be two SRV lookups
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [call(b"_matrix-fed._tcp.testserv"), call(b"_matrix._tcp.testserv")]
         )
 
         # we should fall back to a direct connection
@@ -788,9 +788,12 @@ class MatrixFederationAgentTests(unittest.TestCase):
             content=b'{ "m.server": "target-server" }',
         )
 
-        # there should be a SRV lookup
-        self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.target-server"
+        # there should be two SRV lookups
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [
+                call(b"_matrix-fed._tcp.target-server"),
+                call(b"_matrix._tcp.target-server"),
+            ]
         )
 
         # now we should get a connection to the target server
@@ -878,9 +881,12 @@ class MatrixFederationAgentTests(unittest.TestCase):
 
         self.reactor.pump((0.1,))
 
-        # there should be a SRV lookup
-        self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.target-server"
+        # there should be two SRV lookups
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [
+                call(b"_matrix-fed._tcp.target-server"),
+                call(b"_matrix._tcp.target-server"),
+            ]
         )
 
         # now we should get a connection to the target server
@@ -942,9 +948,9 @@ class MatrixFederationAgentTests(unittest.TestCase):
             client_factory, expected_sni=b"testserv", content=b"NOT JSON"
         )
 
-        # now there should be a SRV lookup
-        self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.testserv"
+        # now there should be two SRV lookups
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [call(b"_matrix-fed._tcp.testserv"), call(b"_matrix._tcp.testserv")]
         )
 
         # we should fall back to a direct connection
@@ -1016,14 +1022,14 @@ class MatrixFederationAgentTests(unittest.TestCase):
         # there should be no requests
         self.assertEqual(len(http_proto.requests), 0)
 
-        # and there should be a SRV lookup instead
-        self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.testserv"
+        # and there should be two SRV lookups instead
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [call(b"_matrix-fed._tcp.testserv"), call(b"_matrix._tcp.testserv")]
         )
 
     def test_get_hostname_srv(self) -> None:
         """
-        Test the behaviour when there is a single SRV record
+        Test the behaviour when there is a single SRV record for _matrix-fed.
         """
         self.agent = self._make_agent()
 
@@ -1039,7 +1045,51 @@ class MatrixFederationAgentTests(unittest.TestCase):
 
         # the request for a .well-known will have failed with a DNS lookup error.
         self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.testserv"
+            b"_matrix-fed._tcp.testserv"
+        )
+
+        # Make sure treq is trying to connect
+        clients = self.reactor.tcpClients
+        self.assertEqual(len(clients), 1)
+        (host, port, client_factory, _timeout, _bindAddress) = clients[0]
+        self.assertEqual(host, "1.2.3.4")
+        self.assertEqual(port, 8443)
+
+        # make a test server, and wire up the client
+        http_server = self._make_connection(client_factory, expected_sni=b"testserv")
+
+        self.assertEqual(len(http_server.requests), 1)
+        request = http_server.requests[0]
+        self.assertEqual(request.method, b"GET")
+        self.assertEqual(request.path, b"/foo/bar")
+        self.assertEqual(request.requestHeaders.getRawHeaders(b"host"), [b"testserv"])
+
+        # finish the request
+        request.finish()
+        self.reactor.pump((0.1,))
+        self.successResultOf(test_d)
+
+    def test_get_hostname_srv_legacy(self) -> None:
+        """
+        Test the behaviour when there is a single SRV record for _matrix.
+        """
+        self.agent = self._make_agent()
+
+        # Return no entries for the _matrix-fed lookup, and a response for _matrix.
+        self.mock_resolver.resolve_service.side_effect = [
+            [],
+            [Server(host=b"srvtarget", port=8443)],
+        ]
+        self.reactor.lookups["srvtarget"] = "1.2.3.4"
+
+        test_d = self._make_get_request(b"matrix-federation://testserv/foo/bar")
+
+        # Nothing happened yet
+        self.assertNoResult(test_d)
+
+        # the request for a .well-known will have failed with a DNS lookup error.
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [call(b"_matrix-fed._tcp.testserv"), call(b"_matrix._tcp.testserv")]
         )
 
         # Make sure treq is trying to connect
@@ -1065,7 +1115,7 @@ class MatrixFederationAgentTests(unittest.TestCase):
 
     def test_get_well_known_srv(self) -> None:
         """Test the behaviour when the .well-known redirects to a place where there
-        is a SRV.
+        is a _matrix-fed SRV record.
         """
         self.agent = self._make_agent()
 
@@ -1096,7 +1146,72 @@ class MatrixFederationAgentTests(unittest.TestCase):
 
         # there should be a SRV lookup
         self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.target-server"
+            b"_matrix-fed._tcp.target-server"
+        )
+
+        # now we should get a connection to the target of the SRV record
+        self.assertEqual(len(clients), 2)
+        (host, port, client_factory, _timeout, _bindAddress) = clients[1]
+        self.assertEqual(host, "5.6.7.8")
+        self.assertEqual(port, 8443)
+
+        # make a test server, and wire up the client
+        http_server = self._make_connection(
+            client_factory, expected_sni=b"target-server"
+        )
+
+        self.assertEqual(len(http_server.requests), 1)
+        request = http_server.requests[0]
+        self.assertEqual(request.method, b"GET")
+        self.assertEqual(request.path, b"/foo/bar")
+        self.assertEqual(
+            request.requestHeaders.getRawHeaders(b"host"), [b"target-server"]
+        )
+
+        # finish the request
+        request.finish()
+        self.reactor.pump((0.1,))
+        self.successResultOf(test_d)
+
+    def test_get_well_known_srv_legacy(self) -> None:
+        """Test the behaviour when the .well-known redirects to a place where there
+        is a _matrix SRV record.
+        """
+        self.agent = self._make_agent()
+
+        self.reactor.lookups["testserv"] = "1.2.3.4"
+        self.reactor.lookups["srvtarget"] = "5.6.7.8"
+
+        test_d = self._make_get_request(b"matrix-federation://testserv/foo/bar")
+
+        # Nothing happened yet
+        self.assertNoResult(test_d)
+
+        # there should be an attempt to connect on port 443 for the .well-known
+        clients = self.reactor.tcpClients
+        self.assertEqual(len(clients), 1)
+        (host, port, client_factory, _timeout, _bindAddress) = clients[0]
+        self.assertEqual(host, "1.2.3.4")
+        self.assertEqual(port, 443)
+
+        # Return no entries for the _matrix-fed lookup, and a response for _matrix.
+        self.mock_resolver.resolve_service.side_effect = [
+            [],
+            [Server(host=b"srvtarget", port=8443)],
+        ]
+
+        self._handle_well_known_connection(
+            client_factory,
+            expected_sni=b"testserv",
+            content=b'{ "m.server": "target-server" }',
+        )
+
+        # there should be two SRV lookups
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [
+                call(b"_matrix-fed._tcp.target-server"),
+                call(b"_matrix._tcp.target-server"),
+            ]
         )
 
         # now we should get a connection to the target of the SRV record
@@ -1158,8 +1273,11 @@ class MatrixFederationAgentTests(unittest.TestCase):
         self.reactor.pump((0.4,))
 
         # now there should have been a SRV lookup
-        self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.xn--bcher-kva.com"
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [
+                call(b"_matrix-fed._tcp.xn--bcher-kva.com"),
+                call(b"_matrix._tcp.xn--bcher-kva.com"),
+            ]
         )
 
         # We should fall back to port 8448
@@ -1188,7 +1306,7 @@ class MatrixFederationAgentTests(unittest.TestCase):
         self.successResultOf(test_d)
 
     def test_idna_srv_target(self) -> None:
-        """test the behaviour when the target of a SRV record has idna chars"""
+        """test the behaviour when the target of a _matrix-fed SRV record has idna chars"""
         self.agent = self._make_agent()
 
         self.mock_resolver.resolve_service.return_value = [
@@ -1204,7 +1322,57 @@ class MatrixFederationAgentTests(unittest.TestCase):
         self.assertNoResult(test_d)
 
         self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.xn--bcher-kva.com"
+            b"_matrix-fed._tcp.xn--bcher-kva.com"
+        )
+
+        # Make sure treq is trying to connect
+        clients = self.reactor.tcpClients
+        self.assertEqual(len(clients), 1)
+        (host, port, client_factory, _timeout, _bindAddress) = clients[0]
+        self.assertEqual(host, "1.2.3.4")
+        self.assertEqual(port, 8443)
+
+        # make a test server, and wire up the client
+        http_server = self._make_connection(
+            client_factory, expected_sni=b"xn--bcher-kva.com"
+        )
+
+        self.assertEqual(len(http_server.requests), 1)
+        request = http_server.requests[0]
+        self.assertEqual(request.method, b"GET")
+        self.assertEqual(request.path, b"/foo/bar")
+        self.assertEqual(
+            request.requestHeaders.getRawHeaders(b"host"), [b"xn--bcher-kva.com"]
+        )
+
+        # finish the request
+        request.finish()
+        self.reactor.pump((0.1,))
+        self.successResultOf(test_d)
+
+    def test_idna_srv_target_legacy(self) -> None:
+        """test the behaviour when the target of a _matrix SRV record has idna chars"""
+        self.agent = self._make_agent()
+
+        # Return no entries for the _matrix-fed lookup, and a response for _matrix.
+        self.mock_resolver.resolve_service.side_effect = [
+            [],
+            [Server(host=b"xn--trget-3qa.com", port=8443)],
+        ]  # târget.com
+        self.reactor.lookups["xn--trget-3qa.com"] = "1.2.3.4"
+
+        test_d = self._make_get_request(
+            b"matrix-federation://xn--bcher-kva.com/foo/bar"
+        )
+
+        # Nothing happened yet
+        self.assertNoResult(test_d)
+
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [
+                call(b"_matrix-fed._tcp.xn--bcher-kva.com"),
+                call(b"_matrix._tcp.xn--bcher-kva.com"),
+            ]
         )
 
         # Make sure treq is trying to connect
@@ -1394,7 +1562,7 @@ class MatrixFederationAgentTests(unittest.TestCase):
         self.assertIsNone(r.delegated_server)
 
     def test_srv_fallbacks(self) -> None:
-        """Test that other SRV results are tried if the first one fails."""
+        """Test that other SRV results are tried if the first one fails for _matrix-fed SRV."""
         self.agent = self._make_agent()
 
         self.mock_resolver.resolve_service.return_value = [
@@ -1409,7 +1577,7 @@ class MatrixFederationAgentTests(unittest.TestCase):
         self.assertNoResult(test_d)
 
         self.mock_resolver.resolve_service.assert_called_once_with(
-            b"_matrix._tcp.testserv"
+            b"_matrix-fed._tcp.testserv"
         )
 
         # We should see an attempt to connect to the first server
@@ -1449,6 +1617,103 @@ class MatrixFederationAgentTests(unittest.TestCase):
         self.reactor.pump((0.1,))
         self.successResultOf(test_d)
 
+    def test_srv_fallbacks_legacy(self) -> None:
+        """Test that other SRV results are tried if the first one fails for _matrix SRV."""
+        self.agent = self._make_agent()
+
+        # Return no entries for the _matrix-fed lookup, and a response for _matrix.
+        self.mock_resolver.resolve_service.side_effect = [
+            [],
+            [
+                Server(host=b"target.com", port=8443),
+                Server(host=b"target.com", port=8444),
+            ],
+        ]
+        self.reactor.lookups["target.com"] = "1.2.3.4"
+
+        test_d = self._make_get_request(b"matrix-federation://testserv/foo/bar")
+
+        # Nothing happened yet
+        self.assertNoResult(test_d)
+
+        self.mock_resolver.resolve_service.assert_has_calls(
+            [call(b"_matrix-fed._tcp.testserv"), call(b"_matrix._tcp.testserv")]
+        )
+
+        # We should see an attempt to connect to the first server
+        clients = self.reactor.tcpClients
+        self.assertEqual(len(clients), 1)
+        (host, port, client_factory, _timeout, _bindAddress) = clients.pop(0)
+        self.assertEqual(host, "1.2.3.4")
+        self.assertEqual(port, 8443)
+
+        # Fonx the connection
+        client_factory.clientConnectionFailed(None, Exception("nope"))
+
+        # There's a 300ms delay in HostnameEndpoint
+        self.reactor.pump((0.4,))
+
+        # Hasn't failed yet
+        self.assertNoResult(test_d)
+
+        # We shouldnow see an attempt to connect to the second server
+        clients = self.reactor.tcpClients
+        self.assertEqual(len(clients), 1)
+        (host, port, client_factory, _timeout, _bindAddress) = clients.pop(0)
+        self.assertEqual(host, "1.2.3.4")
+        self.assertEqual(port, 8444)
+
+        # make a test server, and wire up the client
+        http_server = self._make_connection(client_factory, expected_sni=b"testserv")
+
+        self.assertEqual(len(http_server.requests), 1)
+        request = http_server.requests[0]
+        self.assertEqual(request.method, b"GET")
+        self.assertEqual(request.path, b"/foo/bar")
+        self.assertEqual(request.requestHeaders.getRawHeaders(b"host"), [b"testserv"])
+
+        # finish the request
+        request.finish()
+        self.reactor.pump((0.1,))
+        self.successResultOf(test_d)
+
+    def test_srv_no_fallback_to_legacy(self) -> None:
+        """Test that _matrix SRV results are not tried if the _matrix-fed one fails."""
+        self.agent = self._make_agent()
+
+        # Return a failing entry for _matrix-fed.
+        self.mock_resolver.resolve_service.side_effect = [
+            [Server(host=b"target.com", port=8443)],
+            [],
+        ]
+        self.reactor.lookups["target.com"] = "1.2.3.4"
+
+        test_d = self._make_get_request(b"matrix-federation://testserv/foo/bar")
+
+        # Nothing happened yet
+        self.assertNoResult(test_d)
+
+        # Only the _matrix-fed is checked, _matrix is ignored.
+        self.mock_resolver.resolve_service.assert_called_once_with(
+            b"_matrix-fed._tcp.testserv"
+        )
+
+        # We should see an attempt to connect to the first server
+        clients = self.reactor.tcpClients
+        self.assertEqual(len(clients), 1)
+        (host, port, client_factory, _timeout, _bindAddress) = clients.pop(0)
+        self.assertEqual(host, "1.2.3.4")
+        self.assertEqual(port, 8443)
+
+        # Fonx the connection
+        client_factory.clientConnectionFailed(None, Exception("nope"))
+
+        # There's a 300ms delay in HostnameEndpoint
+        self.reactor.pump((0.4,))
+
+        # Failed to resolve a server.
+        self.assertFailure(test_d, Exception)
+
 
 class TestCachePeriodFromHeaders(unittest.TestCase):
     def test_cache_control(self) -> None: