diff --git a/lightningd/plugin_control.c b/lightningd/plugin_control.c
index a5b83c8e9..0ed7f951e 100644
--- a/lightningd/plugin_control.c
+++ b/lightningd/plugin_control.c
@@ -32,6 +32,9 @@ static struct command_result *plugin_dynamic_list_plugins(struct command *cmd)
 	return command_success(cmd, response);
 }
 
+/* Mutual recursion. */
+static void plugin_dynamic_crash(struct plugin *plugin, struct dynamic_plugin *dp);
+
 /**
  * Returned by all subcommands on error.
  */
@@ -42,6 +45,8 @@ plugin_dynamic_error(struct dynamic_plugin *dp, const char *error)
 		plugin_kill(dp->plugin, "%s", error);
 	else
 		log_info(dp->cmd->ld->log, "%s", error);
+
+	tal_del_destructor2(dp->plugin, plugin_dynamic_crash, dp);
 	return command_fail(dp->cmd, JSONRPC2_INVALID_PARAMS,
 	                    "%s: %s", dp->plugin ? dp->plugin->cmd : "unknown plugin",
 	                    error);
@@ -52,6 +57,11 @@ static void plugin_dynamic_timeout(struct dynamic_plugin *dp)
 	plugin_dynamic_error(dp, "Timed out while waiting for plugin response");
 }
 
+static void plugin_dynamic_crash(struct plugin *p, struct dynamic_plugin *dp)
+{
+	plugin_dynamic_error(dp, "Plugin exited before completing handshake.");
+}
+
 static void plugin_dynamic_config_callback(const char *buffer,
                                            const jsmntok_t *toks,
                                            const jsmntok_t *idtok,
@@ -63,6 +73,7 @@ static void plugin_dynamic_config_callback(const char *buffer,
 	/* Reset the timer only now so that we are either configured, or
 	 * killed. */
 	tal_free(dp->plugin->timeout_timer);
+	tal_del_destructor2(dp->plugin, plugin_dynamic_crash, dp);
 
 	list_for_each(&dp->plugin->plugins->plugins, p, list) {
 		if (p->plugin_state != CONFIGURED)
@@ -133,9 +144,21 @@ static struct command_result *plugin_start(struct dynamic_plugin *dp)
 	/* Give the plugin 20 seconds to respond to `getmanifest`, so we don't hang
 	 * too long on the RPC caller. */
 	p->timeout_timer = new_reltimer(dp->cmd->ld->timers, dp,
-	                                time_from_sec((10)),
+	                                time_from_sec((20)),
 	                                plugin_dynamic_timeout, dp);
 
+	/* Besides the timeout we could also have the plugin crash before
+	 * completing the handshake. In that case we'll get notified and we
+	 * can clean up the `struct dynamic_plugin` and return an appropriate
+	 * error.
+	 *
+	 * The destructor is deregistered in the following places:
+	 *
+	 *  - plugin_dynamic_error in case of a timeout or a crash
+	 *  - plugin_dynamic_config_callback if the handshake completes
+	 */
+	tal_add_destructor2(p, plugin_dynamic_crash, dp);
+
 	/* Create two connections, one read-only on top of the plugin's stdin, and one
 	 * write-only on its stdout. */
 	io_new_conn(p, stdout, plugin_stdout_conn_init, p);
diff --git a/tests/plugins/slow_init.py b/tests/plugins/slow_init.py
index 48c279047..8587531be 100755
--- a/tests/plugins/slow_init.py
+++ b/tests/plugins/slow_init.py
@@ -8,7 +8,7 @@ plugin = Plugin()
 @plugin.init()
 def init(options, configuration, plugin):
     plugin.log("slow_init.py initializing {}".format(configuration))
-    time.sleep(11)
+    time.sleep(21)
 
 
 plugin.run()
diff --git a/tests/test_plugin.py b/tests/test_plugin.py
index 7a3920e95..806f2abfd 100644
--- a/tests/test_plugin.py
+++ b/tests/test_plugin.py
@@ -161,7 +161,7 @@ def test_plugin_command(node_factory):
         n2.rpc.plugin_stop(plugin="static.py")
 
     # Test that we don't crash when starting a broken plugin
-    with pytest.raises(RpcError, match=r"Timed out while waiting for plugin response"):
+    with pytest.raises(RpcError, match=r"Plugin exited before completing handshake."):
         n2.rpc.plugin_start(plugin=os.path.join(os.getcwd(), "tests/plugins/broken.py"))