diff --git a/federation/server.go b/federation/server.go
index 3e0ed3cf..36487a1a 100644
--- a/federation/server.go
+++ b/federation/server.go
@@ -528,7 +528,88 @@ func (s *Server) Mux() *mux.Router {
 	return s.mux
 }
 
-// Listen for federation server requests - call the returned function to gracefully close the server.
+// Keep track of the ports that we've previously used so that we never use the same port
+// (and therefore the same `server_name`) to two different servers.
+//
+// A `Server` is identified over federation solely by its `server_name` (which looks
+// like `hostname:port` for these Complement engineered homeservers). When the OS recycles a
+// freed port, a new Server could otherwise get a `server_name` that is identical to a
+// previously torn-down one.
+//
+// To explain an actual situation where this becomes a problem: A real homeserver under
+// test (that is participating in a room with the now-dead engineered homeserver) might
+// still try to reach the dead server, but since the `server_name` is the same, it's now
+// hitting the new server unexpectedly (cross-test pollution).
+//
+// This particularly happens when you try to share a `deployment` across many tests and
+// then each test creates a engineered homeservers to interact against.
+//
+// Retiring each port for the lifetime of the process keeps stray requests pointed at a
+// dead port (connection refused) instead of a live, unrelated server.
+var (
+	// Use a mutex so only one thread can advance `lastUsedPort` at a time. We don't want
+	// multiple threads clobbering `lastUsedPort`.
+	lastUsedPortMu sync.Mutex
+	// Start at 1024 (1023 + 1) to avoid the priviged ports used by the system
+	//
+	// Since we sequentially try each port, we just need to keep track of the last one we tried
+	lastUsedPort = 1023
+)
+
+// listenOnUnusedPort listens on an unused port that no other federation `Server` has
+// used before in this process.
+func listenOnUnusedPort(t ct.TestLike) net.Listener {
+	lastUsedPortMu.Lock()
+	defer lastUsedPortMu.Unlock()
+
+	// We use this sequential port scan strategy over guess and check with an OS-assigned
+	// port (by using `:0`) as it's more efficient. The OS may recycle and re-use freed
+	// ports meaning we could regress to O(n^2) behavior trying to search for each new
+	// port we want to find.
+	//
+	// Using `:0` means an unused port is automatically picked for us (could be random,
+	// could be the next sequential unused port, we don't know). Ideally, we could ask for
+	// the next unused port after X to avoid a bunch of work. When using using `:0`, the
+	// pathological case that is O(n^2) is if OS hands back next lowest unused port
+	// sequentially which would mean we would have to probe and hold each listener until
+	// we finally got something new.
+
+	// Try the whole port range (untested but it's probably fast to do so)
+	max_attempts := 65535
+	var lastErr error
+	for i := 0; i < max_attempts; i++ {
+		port := lastUsedPort + 1
+		if port > 65535 {
+			// If this ever becomes a problem, we can namespace used ports by `deployment` since
+			// that has to be passed into `NewServer(...)` anyway and the whole point of this is
+			// that a homeserver from the `deployment` doesn't try to reach out to a previous
+			// engineered homeserver it knows about.
+			//
+			// As another alternative, we could also wrap-around to the beginning of the port
+			// range again although that is slightly unsound.
+			ct.Fatalf(
+				t, "listenOnUnusedPort: could not find an unused port in the entire port range (0 - 65535). "+
+					"(see comment here if you run into this). Last error: %s", lastErr,
+			)
+		}
+
+		// Check port availability
+		ln, err := net.Listen("tcp", fmt.Sprintf(":%d", port))
+		lastUsedPort = port
+		if err != nil {
+			lastErr = err
+			// Port unavailable, skip
+			continue
+		}
+
+		return ln
+	}
+	// Since we try the entire port range, we don't really expect to get here but we have
+	// it in case there is a programming error above
+	ct.Fatalf(t, "listenOnUnusedPort: Programming error")
+	return nil
+}
+
 func (s *Server) Listen() (cancel func()) {
 	if s.listening {
 		return
@@ -536,10 +617,7 @@ func (s *Server) Listen() (cancel func()) {
 	var wg sync.WaitGroup
 	wg.Add(1)
 
-	ln, err := net.Listen("tcp", ":0") //nolint
-	if err != nil {
-		ct.Fatalf(s.t, "ListenFederationServer: net.Listen failed: %s", err)
-	}
+	ln := listenOnUnusedPort(s.t)
 	port := ln.Addr().(*net.TCPAddr).Port
 	s.serverName = spec.ServerName(fmt.Sprintf("%s:%d", s.serverName, port))
 	s.listening = true