Got it working.

backend/drm/backend.c

@@ -47,12 +47,13 @@ static void device_paused(struct wl_listener *listener, void *data) {
 }
 
 static void device_resumed(struct wl_listener *listener, void *data) {
-	struct wlr_backend_state *drm = wl_container_of(listener, drm, device_paused);
+	struct wlr_backend_state *drm = wl_container_of(listener, drm, device_resumed);
 	int *new_fd = data;
 
-	close(drm->fd);
-	drm->fd = *new_fd;
-	drm->renderer.fd = *new_fd;
+	if (dup2(*new_fd, drm->fd) < 0) {
+		wlr_log(L_ERROR, "dup2 failed: %s", strerror(errno));
+		return;
+	}
 
 	for (size_t i = 0; i < drm->outputs->length; ++i) {
 		struct wlr_output_state *output = drm->outputs->items[i];

session/logind.c

@@ -226,15 +226,6 @@ static int resume_device(sd_bus_message *msg, void *userdata, sd_bus_error *ret_
 		goto error;
 	}
 
-	// The original fd seem to be closed when the message is freed
-	// so we just clone it.
-	fd = fcntl(fd, F_DUPFD_CLOEXEC, 0);
-	if (fd == -1) {
-		wlr_log(L_ERROR, "Failed to clone file descriptor for ResumeDevice: %s",
-			strerror(errno));
-		goto error;
-	}
-
 	// TODO: Use major/minor to make sure the right devices are getting signals
 
 	wl_signal_emit(&session->base.device_resumed, &fd);