diff --git a/block/src/qcow/mod.rs b/block/src/qcow/mod.rs
index 5f91aa3bd..99c808309 100644
--- a/block/src/qcow/mod.rs
+++ b/block/src/qcow/mod.rs
@@ -231,7 +231,8 @@ bitflags! {
 
 impl IncompatFeatures {
     /// Features supported by this implementation.
-    const SUPPORTED: IncompatFeatures = IncompatFeatures::COMPRESSION;
+    const SUPPORTED: IncompatFeatures =
+        IncompatFeatures::DIRTY.union(IncompatFeatures::COMPRESSION);
 
     /// Get the fallback name for a known feature bit.
     fn flag_name(bit: u8) -> Option<&'static str> {
@@ -680,6 +681,39 @@ impl QcowHeader {
 
         Ok(())
     }
+
+    /// Write only the incompatible_features field to the file at its fixed offset.
+    fn write_incompatible_features<F: Seek + Write>(&self, file: &mut F) -> Result<()> {
+        if self.version != 3 {
+            return Ok(());
+        }
+        file.seek(SeekFrom::Start(V2_BARE_HEADER_SIZE as u64))
+            .map_err(Error::WritingHeader)?;
+        file.write_u64::<BigEndian>(self.incompatible_features)
+            .map_err(Error::WritingHeader)?;
+        Ok(())
+    }
+
+    /// Set or clear the dirty bit for QCOW2 v3 images.
+    ///
+    /// When `dirty` is true, sets the bit to indicate the image is in use.
+    /// When `dirty` is false, clears the bit to indicate a clean shutdown.
+    pub fn set_dirty_bit<F: Seek + Write + FileSync>(
+        &mut self,
+        file: &mut F,
+        dirty: bool,
+    ) -> Result<()> {
+        if self.version == 3 {
+            if dirty {
+                self.incompatible_features |= IncompatFeatures::DIRTY.bits();
+            } else {
+                self.incompatible_features &= !IncompatFeatures::DIRTY.bits();
+            }
+            self.write_incompatible_features(file)?;
+            file.fsync().map_err(Error::WritingHeader)?;
+        }
+        Ok(())
+    }
 }
 
 fn max_refcount_clusters(refcount_order: u32, cluster_size: u32, num_clusters: u32) -> u64 {
@@ -892,7 +926,18 @@ impl QcowFile {
 
         let mut raw_file = QcowRawFile::from(file, cluster_size, refcount_bits)
             .ok_or(Error::InvalidClusterSize)?;
-        if refcount_rebuild_required {
+        let is_writable = raw_file.file().is_writable();
+
+        // Image already has dirty bit set. Refcounts may be invalid.
+        if IncompatFeatures::from_bits_truncate(header.incompatible_features)
+            .contains(IncompatFeatures::DIRTY)
+        {
+            log::warn!("QCOW2 image not cleanly closed, rebuilding refcounts");
+            refcount_rebuild_required = true;
+        }
+
+        // Skip refcount rebuilding for readonly files.
+        if refcount_rebuild_required && is_writable {
             QcowFile::rebuild_refcounts(&mut raw_file, header.clone())?;
         }
 
@@ -965,6 +1010,13 @@ impl QcowFile {
 
         qcow.find_avail_clusters()?;
 
+        if !IncompatFeatures::from_bits_truncate(qcow.header.incompatible_features)
+            .contains(IncompatFeatures::DIRTY)
+            && is_writable
+        {
+            qcow.header.set_dirty_bit(qcow.raw_file.file_mut(), true)?;
+        }
+
         Ok(qcow)
     }
 
@@ -1999,6 +2051,7 @@ impl QcowFile {
         if sync_required {
             self.raw_file.file_mut().sync_data()?;
         }
+
         Ok(())
     }
 }
@@ -2012,6 +2065,9 @@ impl AsRawFd for QcowFile {
 impl Drop for QcowFile {
     fn drop(&mut self) {
         let _ = self.sync_caches();
+        if self.raw_file.file().is_writable() {
+            let _ = self.header.set_dirty_bit(self.raw_file.file_mut(), false);
+        }
     }
 }
 
diff --git a/block/src/qcow/qcow_raw_file.rs b/block/src/qcow/qcow_raw_file.rs
index 5b8cf7356..af9823306 100644
--- a/block/src/qcow/qcow_raw_file.rs
+++ b/block/src/qcow/qcow_raw_file.rs
@@ -276,6 +276,11 @@ impl QcowRawFile {
         Ok(Some(new_cluster_address))
     }
 
+    /// Returns a reference to the underlying file.
+    pub fn file(&self) -> &RawFile {
+        &self.file
+    }
+
     /// Returns a mutable reference to the underlying file.
     pub fn file_mut(&mut self) -> &mut RawFile {
         &mut self.file
diff --git a/block/src/qcow/raw_file.rs b/block/src/qcow/raw_file.rs
index b80a30adc..eda7751c3 100644
--- a/block/src/qcow/raw_file.rs
+++ b/block/src/qcow/raw_file.rs
@@ -15,6 +15,7 @@ use std::os::unix::io::{AsRawFd, RawFd};
 use std::slice;
 
 use libc::c_void;
+use vmm_sys_util::file_traits::FileSync;
 use vmm_sys_util::seek_hole::SeekHole;
 use vmm_sys_util::write_zeroes::{PunchHole, WriteZeroesAt};
 
@@ -122,6 +123,17 @@ impl RawFile {
     pub fn is_direct(&self) -> bool {
         self.direct_io
     }
+
+    /// Returns true if the file was opened with write access.
+    pub fn is_writable(&self) -> bool {
+        // SAFETY: fcntl with F_GETFL is safe and doesn't modify the file descriptor
+        let flags = unsafe { libc::fcntl(self.file.as_raw_fd(), libc::F_GETFL) };
+        if flags < 0 {
+            return false;
+        }
+        let access_mode = flags & libc::O_ACCMODE;
+        access_mode == libc::O_WRONLY || access_mode == libc::O_RDWR
+    }
 }
 
 impl Read for RawFile {
@@ -327,6 +339,12 @@ impl PunchHole for RawFile {
     }
 }
 
+impl FileSync for RawFile {
+    fn fsync(&mut self) -> std::io::Result<()> {
+        self.file.fsync()
+    }
+}
+
 impl SeekHole for RawFile {
     fn seek_hole(&mut self, offset: u64) -> std::io::Result<Option<u64>> {
         match self.file.seek_hole(offset) {