diff --git a/hw/virtio/vhost-user.c b/hw/virtio/vhost-user.c
index 8dcf049d42..1e7553352a 100644
--- a/hw/virtio/vhost-user.c
+++ b/hw/virtio/vhost-user.c
@@ -2500,10 +2500,9 @@ vhost_user_crypto_close_session(struct vhost_dev *dev, uint64_t session_id)
     return 0;
 }
 
-static bool vhost_user_mem_section_filter(struct vhost_dev *dev,
-                                          MemoryRegionSection *section)
+static bool vhost_user_no_private_memslots(struct vhost_dev *dev)
 {
-    return memory_region_get_fd(section->mr) >= 0;
+    return true;
 }
 
 static int vhost_user_get_inflight_fd(struct vhost_dev *dev,
@@ -2746,6 +2745,7 @@ const VhostOps user_ops = {
         .vhost_backend_init = vhost_user_backend_init,
         .vhost_backend_cleanup = vhost_user_backend_cleanup,
         .vhost_backend_memslots_limit = vhost_user_memslots_limit,
+        .vhost_backend_no_private_memslots = vhost_user_no_private_memslots,
         .vhost_set_log_base = vhost_user_set_log_base,
         .vhost_set_mem_table = vhost_user_set_mem_table,
         .vhost_set_vring_addr = vhost_user_set_vring_addr,
@@ -2772,7 +2772,6 @@ const VhostOps user_ops = {
         .vhost_set_config = vhost_user_set_config,
         .vhost_crypto_create_session = vhost_user_crypto_create_session,
         .vhost_crypto_close_session = vhost_user_crypto_close_session,
-        .vhost_backend_mem_section_filter = vhost_user_mem_section_filter,
         .vhost_get_inflight_fd = vhost_user_get_inflight_fd,
         .vhost_set_inflight_fd = vhost_user_set_inflight_fd,
         .vhost_dev_start = vhost_user_dev_start,
diff --git a/hw/virtio/vhost.c b/hw/virtio/vhost.c
index e2f6ffb446..c1e6148833 100644
--- a/hw/virtio/vhost.c
+++ b/hw/virtio/vhost.c
@@ -45,20 +45,33 @@
 static struct vhost_log *vhost_log;
 static struct vhost_log *vhost_log_shm;
 
+/* Memslots used by backends that support private memslots (without an fd). */
 static unsigned int used_memslots;
+
+/* Memslots used by backends that only support shared memslots (with an fd). */
+static unsigned int used_shared_memslots;
+
 static QLIST_HEAD(, vhost_dev) vhost_devices =
     QLIST_HEAD_INITIALIZER(vhost_devices);
 
 bool vhost_has_free_slot(void)
 {
-    unsigned int slots_limit = ~0U;
+    unsigned int free = UINT_MAX;
     struct vhost_dev *hdev;
 
     QLIST_FOREACH(hdev, &vhost_devices, entry) {
         unsigned int r = hdev->vhost_ops->vhost_backend_memslots_limit(hdev);
-        slots_limit = MIN(slots_limit, r);
+        unsigned int cur_free;
+
+        if (hdev->vhost_ops->vhost_backend_no_private_memslots &&
+            hdev->vhost_ops->vhost_backend_no_private_memslots(hdev)) {
+            cur_free = r - used_shared_memslots;
+        } else {
+            cur_free = r - used_memslots;
+        }
+        free = MIN(free, cur_free);
     }
-    return slots_limit > used_memslots;
+    return free > 0;
 }
 
 static void vhost_dev_sync_region(struct vhost_dev *dev,
@@ -474,8 +487,7 @@ static int vhost_verify_ring_mappings(struct vhost_dev *dev,
  * vhost_section: identify sections needed for vhost access
  *
  * We only care about RAM sections here (where virtqueue and guest
- * internals accessed by virtio might live). If we find one we still
- * allow the backend to potentially filter it out of our list.
+ * internals accessed by virtio might live).
  */
 static bool vhost_section(struct vhost_dev *dev, MemoryRegionSection *section)
 {
@@ -502,8 +514,16 @@ static bool vhost_section(struct vhost_dev *dev, MemoryRegionSection *section)
             return false;
         }
 
-        if (dev->vhost_ops->vhost_backend_mem_section_filter &&
-            !dev->vhost_ops->vhost_backend_mem_section_filter(dev, section)) {
+        /*
+         * Some backends (like vhost-user) can only handle memory regions
+         * that have an fd (can be mapped into a different process). Filter
+         * the ones without an fd out, if requested.
+         *
+         * TODO: we might have to limit to MAP_SHARED as well.
+         */
+        if (memory_region_get_fd(section->mr) < 0 &&
+            dev->vhost_ops->vhost_backend_no_private_memslots &&
+            dev->vhost_ops->vhost_backend_no_private_memslots(dev)) {
             trace_vhost_reject_section(mr->name, 2);
             return false;
         }
@@ -568,7 +588,14 @@ static void vhost_commit(MemoryListener *listener)
                        dev->n_mem_sections * sizeof dev->mem->regions[0];
     dev->mem = g_realloc(dev->mem, regions_size);
     dev->mem->nregions = dev->n_mem_sections;
-    used_memslots = dev->mem->nregions;
+
+    if (dev->vhost_ops->vhost_backend_no_private_memslots &&
+        dev->vhost_ops->vhost_backend_no_private_memslots(dev)) {
+        used_shared_memslots = dev->mem->nregions;
+    } else {
+        used_memslots = dev->mem->nregions;
+    }
+
     for (i = 0; i < dev->n_mem_sections; i++) {
         struct vhost_memory_region *cur_vmr = dev->mem->regions + i;
         struct MemoryRegionSection *mrs = dev->mem_sections + i;
@@ -1400,6 +1427,7 @@ int vhost_dev_init(struct vhost_dev *hdev, void *opaque,
                    VhostBackendType backend_type, uint32_t busyloop_timeout,
                    Error **errp)
 {
+    unsigned int used;
     uint64_t features;
     int i, r, n_initialized_vqs = 0;
 
@@ -1495,7 +1523,17 @@ int vhost_dev_init(struct vhost_dev *hdev, void *opaque,
     memory_listener_register(&hdev->memory_listener, &address_space_memory);
     QLIST_INSERT_HEAD(&vhost_devices, hdev, entry);
 
-    if (used_memslots > hdev->vhost_ops->vhost_backend_memslots_limit(hdev)) {
+    /*
+     * The listener we registered properly updated the corresponding counter.
+     * So we can trust that these values are accurate.
+     */
+    if (hdev->vhost_ops->vhost_backend_no_private_memslots &&
+        hdev->vhost_ops->vhost_backend_no_private_memslots(hdev)) {
+        used = used_shared_memslots;
+    } else {
+        used = used_memslots;
+    }
+    if (used > hdev->vhost_ops->vhost_backend_memslots_limit(hdev)) {
         error_setg(errp, "vhost backend memory slots limit is less"
                    " than current number of present memory slots");
         r = -EINVAL;
diff --git a/include/hw/virtio/vhost-backend.h b/include/hw/virtio/vhost-backend.h
index 31a251a9f5..df2821ddae 100644
--- a/include/hw/virtio/vhost-backend.h
+++ b/include/hw/virtio/vhost-backend.h
@@ -108,8 +108,7 @@ typedef int (*vhost_crypto_create_session_op)(struct vhost_dev *dev,
 typedef int (*vhost_crypto_close_session_op)(struct vhost_dev *dev,
                                              uint64_t session_id);
 
-typedef bool (*vhost_backend_mem_section_filter_op)(struct vhost_dev *dev,
-                                                MemoryRegionSection *section);
+typedef bool (*vhost_backend_no_private_memslots_op)(struct vhost_dev *dev);
 
 typedef int (*vhost_get_inflight_fd_op)(struct vhost_dev *dev,
                                         uint16_t queue_size,
@@ -138,6 +137,7 @@ typedef struct VhostOps {
     vhost_backend_init vhost_backend_init;
     vhost_backend_cleanup vhost_backend_cleanup;
     vhost_backend_memslots_limit vhost_backend_memslots_limit;
+    vhost_backend_no_private_memslots_op vhost_backend_no_private_memslots;
     vhost_net_set_backend_op vhost_net_set_backend;
     vhost_net_set_mtu_op vhost_net_set_mtu;
     vhost_scsi_set_endpoint_op vhost_scsi_set_endpoint;
@@ -172,7 +172,6 @@ typedef struct VhostOps {
     vhost_set_config_op vhost_set_config;
     vhost_crypto_create_session_op vhost_crypto_create_session;
     vhost_crypto_close_session_op vhost_crypto_close_session;
-    vhost_backend_mem_section_filter_op vhost_backend_mem_section_filter;
     vhost_get_inflight_fd_op vhost_get_inflight_fd;
     vhost_set_inflight_fd_op vhost_set_inflight_fd;
     vhost_dev_start_op vhost_dev_start;
