diff --git a/include/sway/ipc-server.h b/include/sway/ipc-server.h
index dd16a175e..026b55541 100644
--- a/include/sway/ipc-server.h
+++ b/include/sway/ipc-server.h
@@ -9,8 +9,6 @@ struct sway_server;
 
 void ipc_init(struct sway_server *server);
 
-void ipc_terminate(void);
-
 struct sockaddr_un *ipc_user_sockaddr(void);
 
 void ipc_event_workspace(struct sway_container *old,
diff --git a/sway/ipc-server.c b/sway/ipc-server.c
index 3e510c2e1..abc2d7cba 100644
--- a/sway/ipc-server.c
+++ b/sway/ipc-server.c
@@ -31,6 +31,7 @@ static int ipc_socket = -1;
 static struct wl_event_source *ipc_event_source =  NULL;
 static struct sockaddr_un *ipc_sockaddr = NULL;
 static list_t *ipc_client_list = NULL;
+static struct wl_listener ipc_display_destroy;
 
 static const char ipc_magic[] = {'i', '3', '-', 'i', 'p', 'c'};
 
@@ -56,6 +57,22 @@ void ipc_client_disconnect(struct ipc_client *client);
 void ipc_client_handle_command(struct ipc_client *client);
 bool ipc_send_reply(struct ipc_client *client, const char *payload, uint32_t payload_length);
 
+static void handle_display_destroy(struct wl_listener *listener, void *data) {
+	if (ipc_event_source) {
+		wl_event_source_remove(ipc_event_source);
+	}
+	close(ipc_socket);
+	unlink(ipc_sockaddr->sun_path);
+
+	list_free(ipc_client_list);
+
+	if (ipc_sockaddr) {
+		free(ipc_sockaddr);
+	}
+
+	wl_list_remove(&ipc_display_destroy.link);
+}
+
 void ipc_init(struct sway_server *server) {
 	ipc_socket = socket(AF_UNIX, SOCK_STREAM | SOCK_NONBLOCK | SOCK_CLOEXEC, 0);
 	if (ipc_socket == -1) {
@@ -85,24 +102,13 @@ void ipc_init(struct sway_server *server) {
 
 	ipc_client_list = create_list();
 
+	ipc_display_destroy.notify = handle_display_destroy;
+	wl_display_add_destroy_listener(server->wl_display, &ipc_display_destroy);
+
 	ipc_event_source = wl_event_loop_add_fd(server->wl_event_loop, ipc_socket,
 			WL_EVENT_READABLE, ipc_handle_connection, server);
 }
 
-void ipc_terminate(void) {
-	if (ipc_event_source) {
-		wl_event_source_remove(ipc_event_source);
-	}
-	close(ipc_socket);
-	unlink(ipc_sockaddr->sun_path);
-
-	list_free(ipc_client_list);
-
-	if (ipc_sockaddr) {
-		free(ipc_sockaddr);
-	}
-}
-
 struct sockaddr_un *ipc_user_sockaddr(void) {
 	struct sockaddr_un *ipc_sockaddr = malloc(sizeof(struct sockaddr_un));
 	if (ipc_sockaddr == NULL) {
diff --git a/sway/main.c b/sway/main.c
index 8b0b8612e..96e41bbcb 100644
--- a/sway/main.c
+++ b/sway/main.c
@@ -437,8 +437,6 @@ int main(int argc, char **argv) {
 
 	server_fini(&server);
 
-	ipc_terminate();
-
 	if (config) {
 		free_config(config);
 	}