diff --git a/block/qcow2-bitmap.c b/block/qcow2-bitmap.c
index b8e472b3e8..cb596c2a85 100644
--- a/block/qcow2-bitmap.c
+++ b/block/qcow2-bitmap.c
@@ -44,6 +44,8 @@
 
 /* Bitmap directory entry flags */
 #define BME_RESERVED_FLAGS 0xfffffffcU
+#define BME_FLAG_IN_USE (1U << 0)
+#define BME_FLAG_AUTO   (1U << 1)
 
 /* bits [1, 8] U [56, 63] are reserved */
 #define BME_TABLE_ENTRY_RESERVED_MASK 0xff000000000001feULL
@@ -85,6 +87,23 @@ typedef enum BitmapType {
     BT_DIRTY_TRACKING_BITMAP = 1
 } BitmapType;
 
+static inline bool can_write(BlockDriverState *bs)
+{
+    return !bdrv_is_read_only(bs) && !(bdrv_get_flags(bs) & BDRV_O_INACTIVE);
+}
+
+static int update_header_sync(BlockDriverState *bs)
+{
+    int ret;
+
+    ret = qcow2_update_header(bs);
+    if (ret < 0) {
+        return ret;
+    }
+
+    return bdrv_flush(bs);
+}
+
 static int check_table_entry(uint64_t entry, int cluster_size)
 {
     uint64_t offset;
@@ -146,6 +165,120 @@ fail:
     return ret;
 }
 
+/* This function returns the number of disk sectors covered by a single qcow2
+ * cluster of bitmap data. */
+static uint64_t sectors_covered_by_bitmap_cluster(const BDRVQcow2State *s,
+                                                  const BdrvDirtyBitmap *bitmap)
+{
+    uint32_t sector_granularity =
+            bdrv_dirty_bitmap_granularity(bitmap) >> BDRV_SECTOR_BITS;
+
+    return (uint64_t)sector_granularity * (s->cluster_size << 3);
+}
+
+/* load_bitmap_data
+ * @bitmap_table entries must satisfy specification constraints.
+ * @bitmap must be cleared */
+static int load_bitmap_data(BlockDriverState *bs,
+                            const uint64_t *bitmap_table,
+                            uint32_t bitmap_table_size,
+                            BdrvDirtyBitmap *bitmap)
+{
+    int ret = 0;
+    BDRVQcow2State *s = bs->opaque;
+    uint64_t sector, sbc;
+    uint64_t bm_size = bdrv_dirty_bitmap_size(bitmap);
+    uint8_t *buf = NULL;
+    uint64_t i, tab_size =
+            size_to_clusters(s,
+                bdrv_dirty_bitmap_serialization_size(bitmap, 0, bm_size));
+
+    if (tab_size != bitmap_table_size || tab_size > BME_MAX_TABLE_SIZE) {
+        return -EINVAL;
+    }
+
+    buf = g_malloc(s->cluster_size);
+    sbc = sectors_covered_by_bitmap_cluster(s, bitmap);
+    for (i = 0, sector = 0; i < tab_size; ++i, sector += sbc) {
+        uint64_t count = MIN(bm_size - sector, sbc);
+        uint64_t entry = bitmap_table[i];
+        uint64_t offset = entry & BME_TABLE_ENTRY_OFFSET_MASK;
+
+        assert(check_table_entry(entry, s->cluster_size) == 0);
+
+        if (offset == 0) {
+            if (entry & BME_TABLE_ENTRY_FLAG_ALL_ONES) {
+                bdrv_dirty_bitmap_deserialize_ones(bitmap, sector, count,
+                                                   false);
+            } else {
+                /* No need to deserialize zeros because the dirty bitmap is
+                 * already cleared */
+            }
+        } else {
+            ret = bdrv_pread(bs->file, offset, buf, s->cluster_size);
+            if (ret < 0) {
+                goto finish;
+            }
+            bdrv_dirty_bitmap_deserialize_part(bitmap, buf, sector, count,
+                                               false);
+        }
+    }
+    ret = 0;
+
+    bdrv_dirty_bitmap_deserialize_finish(bitmap);
+
+finish:
+    g_free(buf);
+
+    return ret;
+}
+
+static BdrvDirtyBitmap *load_bitmap(BlockDriverState *bs,
+                                    Qcow2Bitmap *bm, Error **errp)
+{
+    int ret;
+    uint64_t *bitmap_table = NULL;
+    uint32_t granularity;
+    BdrvDirtyBitmap *bitmap = NULL;
+
+    if (bm->flags & BME_FLAG_IN_USE) {
+        error_setg(errp, "Bitmap '%s' is in use", bm->name);
+        goto fail;
+    }
+
+    ret = bitmap_table_load(bs, &bm->table, &bitmap_table);
+    if (ret < 0) {
+        error_setg_errno(errp, -ret,
+                         "Could not read bitmap_table table from image for "
+                         "bitmap '%s'", bm->name);
+        goto fail;
+    }
+
+    granularity = 1U << bm->granularity_bits;
+    bitmap = bdrv_create_dirty_bitmap(bs, granularity, bm->name, errp);
+    if (bitmap == NULL) {
+        goto fail;
+    }
+
+    ret = load_bitmap_data(bs, bitmap_table, bm->table.size, bitmap);
+    if (ret < 0) {
+        error_setg_errno(errp, -ret, "Could not read bitmap '%s' from image",
+                         bm->name);
+        goto fail;
+    }
+
+    g_free(bitmap_table);
+    return bitmap;
+
+fail:
+    g_free(bitmap_table);
+    if (bitmap != NULL) {
+        bdrv_release_dirty_bitmap(bs, bitmap);
+    }
+
+    return NULL;
+}
+
 /*
  * Bitmap List
  */
@@ -164,6 +297,15 @@ static inline void bitmap_dir_entry_to_cpu(Qcow2BitmapDirEntry *entry)
     be32_to_cpus(&entry->extra_data_size);
 }
 
+static inline void bitmap_dir_entry_to_be(Qcow2BitmapDirEntry *entry)
+{
+    cpu_to_be64s(&entry->bitmap_table_offset);
+    cpu_to_be32s(&entry->bitmap_table_size);
+    cpu_to_be32s(&entry->flags);
+    cpu_to_be16s(&entry->name_size);
+    cpu_to_be32s(&entry->extra_data_size);
+}
+
 static inline int calc_dir_entry_size(size_t name_size, size_t extra_data_size)
 {
     return align_offset(sizeof(Qcow2BitmapDirEntry) +
@@ -224,6 +366,17 @@ static int check_dir_entry(BlockDriverState *bs, Qcow2BitmapDirEntry *entry)
     return fail ? -EINVAL : 0;
 }
 
+static inline void bitmap_directory_to_be(uint8_t *dir, size_t size)
+{
+    uint8_t *end = dir + size;
+    while (dir < end) {
+        Qcow2BitmapDirEntry *e = (Qcow2BitmapDirEntry *)dir;
+        dir += dir_entry_size(e);
+
+        bitmap_dir_entry_to_be(e);
+    }
+}
+
 /*
  * Bitmap List public functions
  */
@@ -258,6 +411,18 @@ static Qcow2BitmapList *bitmap_list_new(void)
     return bm_list;
 }
 
+static uint32_t bitmap_list_count(Qcow2BitmapList *bm_list)
+{
+    Qcow2Bitmap *bm;
+    uint32_t nb_bitmaps = 0;
+
+    QSIMPLEQ_FOREACH(bm, bm_list, entry) {
+        nb_bitmaps++;
+    }
+
+    return nb_bitmaps;
+}
+
 /* bitmap_list_load
  * Get bitmap list from qcow2 image. Actually reads bitmap directory,
  * checks it and convert to bitmap list.
@@ -437,3 +602,226 @@ out:
 
     return ret;
 }
+
+/* bitmap_list_store
+ * Store bitmap list to qcow2 image as a bitmap directory.
+ * Everything is checked.
+ */
+static int bitmap_list_store(BlockDriverState *bs, Qcow2BitmapList *bm_list,
+                             uint64_t *offset, uint64_t *size, bool in_place)
+{
+    int ret;
+    uint8_t *dir;
+    int64_t dir_offset = 0;
+    uint64_t dir_size = 0;
+    Qcow2Bitmap *bm;
+    Qcow2BitmapDirEntry *e;
+
+    QSIMPLEQ_FOREACH(bm, bm_list, entry) {
+        dir_size += calc_dir_entry_size(strlen(bm->name), 0);
+    }
+
+    if (dir_size == 0 || dir_size > QCOW2_MAX_BITMAP_DIRECTORY_SIZE) {
+        return -EINVAL;
+    }
+
+    if (in_place) {
+        if (*size != dir_size || *offset == 0) {
+            return -EINVAL;
+        }
+
+        dir_offset = *offset;
+    }
+
+    dir = g_try_malloc(dir_size);
+    if (dir == NULL) {
+        return -ENOMEM;
+    }
+
+    e = (Qcow2BitmapDirEntry *)dir;
+    QSIMPLEQ_FOREACH(bm, bm_list, entry) {
+        e->bitmap_table_offset = bm->table.offset;
+        e->bitmap_table_size = bm->table.size;
+        e->flags = bm->flags;
+        e->type = BT_DIRTY_TRACKING_BITMAP;
+        e->granularity_bits = bm->granularity_bits;
+        e->name_size = strlen(bm->name);
+        e->extra_data_size = 0;
+        memcpy(e + 1, bm->name, e->name_size);
+
+        if (check_dir_entry(bs, e) < 0) {
+            ret = -EINVAL;
+            goto fail;
+        }
+
+        e = next_dir_entry(e);
+    }
+
+    bitmap_directory_to_be(dir, dir_size);
+
+    if (!in_place) {
+        dir_offset = qcow2_alloc_clusters(bs, dir_size);
+        if (dir_offset < 0) {
+            ret = dir_offset;
+            goto fail;
+        }
+    }
+
+    ret = qcow2_pre_write_overlap_check(bs, 0, dir_offset, dir_size);
+    if (ret < 0) {
+        goto fail;
+    }
+
+    ret = bdrv_pwrite(bs->file, dir_offset, dir, dir_size);
+    if (ret < 0) {
+        goto fail;
+    }
+
+    g_free(dir);
+
+    if (!in_place) {
+        *size = dir_size;
+        *offset = dir_offset;
+    }
+
+    return 0;
+
+fail:
+    g_free(dir);
+
+    if (!in_place && dir_offset > 0) {
+        qcow2_free_clusters(bs, dir_offset, dir_size, QCOW2_DISCARD_OTHER);
+    }
+
+    return ret;
+}
+
+/*
+ * Bitmap List end
+ */
+
+static int update_ext_header_and_dir_in_place(BlockDriverState *bs,
+                                              Qcow2BitmapList *bm_list)
+{
+    BDRVQcow2State *s = bs->opaque;
+    int ret;
+
+    if (!(s->autoclear_features & QCOW2_AUTOCLEAR_BITMAPS) ||
+        bm_list == NULL || QSIMPLEQ_EMPTY(bm_list) ||
+        bitmap_list_count(bm_list) != s->nb_bitmaps)
+    {
+        return -EINVAL;
+    }
+
+    s->autoclear_features &= ~(uint64_t)QCOW2_AUTOCLEAR_BITMAPS;
+    ret = update_header_sync(bs);
+    if (ret < 0) {
+        /* Two variants are possible here:
+         * 1. Autoclear flag is dropped, all bitmaps will be lost.
+         * 2. Autoclear flag is not dropped, old state is left.
+         */
+        return ret;
+    }
+
+    /* autoclear bit is not set, so we can safely update bitmap directory */
+
+    ret = bitmap_list_store(bs, bm_list, &s->bitmap_directory_offset,
+                            &s->bitmap_directory_size, true);
+    if (ret < 0) {
+        /* autoclear bit is cleared, so all leaked clusters would be removed on
+         * qemu-img check */
+        return ret;
+    }
+
+    ret = update_header_sync(bs);
+    if (ret < 0) {
+        /* autoclear bit is cleared, so all leaked clusters would be removed on
+         * qemu-img check */
+        return ret;
+    }
+
+    s->autoclear_features |= QCOW2_AUTOCLEAR_BITMAPS;
+    return update_header_sync(bs);
+    /* If final update_header_sync() fails, two variants are possible:
+     * 1. Autoclear flag is not set, all bitmaps will be lost.
+     * 2. Autoclear flag is set, header and directory are successfully updated.
+     */
+}
+
+/* for g_slist_foreach for GSList of BdrvDirtyBitmap* elements */
+static void release_dirty_bitmap_helper(gpointer bitmap,
+                                        gpointer bs)
+{
+    bdrv_release_dirty_bitmap(bs, bitmap);
+}
+
+/* for g_slist_foreach for GSList of BdrvDirtyBitmap* elements */
+static void set_readonly_helper(gpointer bitmap, gpointer unused)
+{
+    bdrv_dirty_bitmap_set_readonly(bitmap);
+}
+
+/* qcow2_load_autoloading_dirty_bitmaps()
+ * Return value is a hint for caller: true means that the Qcow2 header was
+ * updated. (false doesn't mean that the header should be updated by the
+ * caller, it just means that updating was not needed or the image cannot be
+ * written to).
+ * On failure the function returns false.
+ */
+bool qcow2_load_autoloading_dirty_bitmaps(BlockDriverState *bs, Error **errp)
+{
+    BDRVQcow2State *s = bs->opaque;
+    Qcow2BitmapList *bm_list;
+    Qcow2Bitmap *bm;
+    GSList *created_dirty_bitmaps = NULL;
+    bool header_updated = false;
+
+    if (s->nb_bitmaps == 0) {
+        /* No bitmaps - nothing to do */
+        return false;
+    }
+
+    bm_list = bitmap_list_load(bs, s->bitmap_directory_offset,
+                               s->bitmap_directory_size, errp);
+    if (bm_list == NULL) {
+        return false;
+    }
+
+    QSIMPLEQ_FOREACH(bm, bm_list, entry) {
+        if ((bm->flags & BME_FLAG_AUTO) && !(bm->flags & BME_FLAG_IN_USE)) {
+            BdrvDirtyBitmap *bitmap = load_bitmap(bs, bm, errp);
+            if (bitmap == NULL) {
+                goto fail;
+            }
+            bm->flags |= BME_FLAG_IN_USE;
+            created_dirty_bitmaps =
+                    g_slist_append(created_dirty_bitmaps, bitmap);
+        }
+    }
+
+    if (created_dirty_bitmaps != NULL) {
+        if (can_write(bs)) {
+            /* in_use flags must be updated */
+            int ret = update_ext_header_and_dir_in_place(bs, bm_list);
+            if (ret < 0) {
+                error_setg_errno(errp, -ret, "Can't update bitmap directory");
+                goto fail;
+            }
+            header_updated = true;
+        } else {
+            g_slist_foreach(created_dirty_bitmaps, set_readonly_helper, NULL);
+        }
+    }
+
+    g_slist_free(created_dirty_bitmaps);
+    bitmap_list_free(bm_list);
+
+    return header_updated;
+
+fail:
+    g_slist_foreach(created_dirty_bitmaps, release_dirty_bitmap_helper, bs);
+    g_slist_free(created_dirty_bitmaps);
+    bitmap_list_free(bm_list);
+
+    return false;
+}
diff --git a/block/qcow2.c b/block/qcow2.c
index 28a16789af..a70d284b75 100644
--- a/block/qcow2.c
+++ b/block/qcow2.c
@@ -1239,9 +1239,22 @@ static int qcow2_do_open(BlockDriverState *bs, QDict *options, int flags,
 
     /* Clear unknown autoclear feature bits */
     update_header |= s->autoclear_features & ~QCOW2_AUTOCLEAR_MASK;
-
-    if (update_header && !bs->read_only && !(flags & BDRV_O_INACTIVE)) {
+    update_header =
+        update_header && !bs->read_only && !(flags & BDRV_O_INACTIVE);
+    if (update_header) {
         s->autoclear_features &= QCOW2_AUTOCLEAR_MASK;
+    }
+
+    if (qcow2_load_autoloading_dirty_bitmaps(bs, &local_err)) {
+        update_header = false;
+    }
+    if (local_err != NULL) {
+        error_propagate(errp, local_err);
+        ret = -EINVAL;
+        goto fail;
+    }
+
+    if (update_header) {
         ret = qcow2_update_header(bs);
         if (ret < 0) {
             error_setg_errno(errp, -ret, "Could not update qcow2 header");
diff --git a/block/qcow2.h b/block/qcow2.h
index f4a1f4cd78..67c61de008 100644
--- a/block/qcow2.h
+++ b/block/qcow2.h
@@ -629,4 +629,6 @@ void qcow2_cache_put(BlockDriverState *bs, Qcow2Cache *c, void **table);
 int qcow2_check_bitmaps_refcounts(BlockDriverState *bs, BdrvCheckResult *res,
                                   void **refcount_table,
                                   int64_t *refcount_table_size);
+bool qcow2_load_autoloading_dirty_bitmaps(BlockDriverState *bs, Error **errp);
+
 #endif
