diff --git a/include/qemu/vhost-user-server.h b/include/qemu/vhost-user-server.h
index 64ad701015..0417ec0533 100644
--- a/include/qemu/vhost-user-server.h
+++ b/include/qemu/vhost-user-server.h
@@ -45,6 +45,7 @@ typedef struct {
     /* Protected by ctx lock */
     bool in_qio_channel_yield;
     bool wait_idle;
+    bool quiescing;
     VuDev vu_dev;
     QIOChannel *ioc; /* The I/O channel with the client */
     QIOChannelSocket *sioc; /* The underlying data channel with the client */
diff --git a/block/export/vhost-user-blk-server.c b/block/export/vhost-user-blk-server.c
index fe2cee3a78..16f48388d3 100644
--- a/block/export/vhost-user-blk-server.c
+++ b/block/export/vhost-user-blk-server.c
@@ -283,6 +283,7 @@ static void vu_blk_drained_begin(void *opaque)
 {
     VuBlkExport *vexp = opaque;
 
+    vexp->vu_server.quiescing = true;
     vhost_user_server_detach_aio_context(&vexp->vu_server);
 }
 
@@ -291,19 +292,23 @@ static void vu_blk_drained_end(void *opaque)
 {
     VuBlkExport *vexp = opaque;
 
+    vexp->vu_server.quiescing = false;
     vhost_user_server_attach_aio_context(&vexp->vu_server, vexp->export.ctx);
 }
 
 /*
- * Ensures that bdrv_drained_begin() waits until in-flight requests complete.
+ * Ensures that bdrv_drained_begin() waits until in-flight requests complete
+ * and the server->co_trip coroutine has terminated. It will be restarted in
+ * vhost_user_server_attach_aio_context().
  *
  * Called with vexp->export.ctx acquired.
  */
 static bool vu_blk_drained_poll(void *opaque)
 {
     VuBlkExport *vexp = opaque;
+    VuServer *server = &vexp->vu_server;
 
-    return vhost_user_server_has_in_flight(&vexp->vu_server);
+    return server->co_trip || vhost_user_server_has_in_flight(server);
 }
 
 static const BlockDevOps vu_blk_dev_ops = {
diff --git a/util/vhost-user-server.c b/util/vhost-user-server.c
index 5ccc6d24a0..a9a48fffb8 100644
--- a/util/vhost-user-server.c
+++ b/util/vhost-user-server.c
@@ -132,8 +132,7 @@ vu_message_read(VuDev *vu_dev, int conn_fd, VhostUserMsg *vmsg)
                     qio_channel_yield(ioc, G_IO_IN);
                     server->in_qio_channel_yield = false;
                 } else {
-                    /* Wait until attached to an AioContext again */
-                    qemu_coroutine_yield();
+                    return false;
                 }
                 continue;
             } else {
@@ -201,8 +200,16 @@ static coroutine_fn void vu_client_trip(void *opaque)
     VuServer *server = opaque;
     VuDev *vu_dev = &server->vu_dev;
 
-    while (!vu_dev->broken && vu_dispatch(vu_dev)) {
-        /* Keep running */
+    while (!vu_dev->broken) {
+        if (server->quiescing) {
+            server->co_trip = NULL;
+            aio_wait_kick();
+            return;
+        }
+        /* vu_dispatch() returns false if server->ctx went away */
+        if (!vu_dispatch(vu_dev) && server->ctx) {
+            break;
+        }
     }
 
     if (vhost_user_server_has_in_flight(server)) {
@@ -353,8 +360,7 @@ static void vu_accept(QIONetListener *listener, QIOChannelSocket *sioc,
 
     qio_channel_set_follow_coroutine_ctx(server->ioc, true);
 
-    server->co_trip = qemu_coroutine_create(vu_client_trip, server);
-
+    /* Attaching the AioContext starts the vu_client_trip coroutine */
     aio_context_acquire(server->ctx);
     vhost_user_server_attach_aio_context(server, server->ctx);
     aio_context_release(server->ctx);
@@ -413,8 +419,25 @@ void vhost_user_server_attach_aio_context(VuServer *server, AioContext *ctx)
                            NULL, NULL, vu_fd_watch);
     }
 
-    assert(!server->in_qio_channel_yield);
-    aio_co_schedule(ctx, server->co_trip);
+    if (server->co_trip) {
+        /*
+         * The caller didn't fully shut down co_trip (this can happen on
+         * non-polling drains like in bdrv_graph_wrlock()). This is okay as long
+         * as it no longer tries to shut it down and we're guaranteed to still
+         * be in the same AioContext as before.
+         *
+         * co_ctx can still be NULL if we get multiple calls and only just
+         * scheduled a new coroutine in the else branch.
+         */
+        AioContext *co_ctx = qemu_coroutine_get_aio_context(server->co_trip);
+
+        assert(!server->quiescing);
+        assert(!co_ctx || co_ctx == ctx);
+    } else {
+        server->co_trip = qemu_coroutine_create(vu_client_trip, server);
+        assert(!server->in_qio_channel_yield);
+        aio_co_schedule(ctx, server->co_trip);
+    }
 }
 
 /* Called with server->ctx acquired */
