diff --git a/tests/overlay-local-store/local.mk b/tests/overlay-local-store/local.mk
index 19ae6a3d0..34056683d 100644
--- a/tests/overlay-local-store/local.mk
+++ b/tests/overlay-local-store/local.mk
@@ -8,6 +8,7 @@ overlay-local-store-tests := \
   $(d)/delete-duplicate.sh \
   $(d)/gc.sh \
   $(d)/verify.sh \
-  $(d)/optimise.sh
+  $(d)/optimise.sh \
+  $(d)/stale-file-handle.sh
 
 install-tests-groups += overlay-local-store
diff --git a/tests/overlay-local-store/stale-file-handle-inner.sh b/tests/overlay-local-store/stale-file-handle-inner.sh
new file mode 100755
index 000000000..86e39fa40
--- /dev/null
+++ b/tests/overlay-local-store/stale-file-handle-inner.sh
@@ -0,0 +1,47 @@
+#!/usr/bin/env bash
+
+set -eu -o pipefail
+
+set -x
+
+source common.sh
+
+# Avoid store dir being inside sandbox build-dir
+unset NIX_STORE_DIR
+unset NIX_STATE_DIR
+
+storeDirs
+
+initLowerStore
+
+mountOverlayfs
+
+buildInStore () {
+    nix-build --store "$1" ../hermetic.nix --arg busybox "$busybox" --arg seed 1 --no-out-link
+}
+
+triggerStaleFileHandle () {
+    # Arrange it so there are duplicate paths
+    nix-store --store "$storeA" --gc  # Clear lower store
+    buildInStore "$storeB"  # Build into upper layer first
+    buildInStore "$storeA"  # Then build in lower store
+
+    # Duplicate paths mean GC will have to delete via upper layer
+    nix-store --store "$storeB" --gc
+
+    # Clear lower store again to force building in upper layer
+    nix-store --store "$storeA" --gc
+
+    # Now attempting to build in upper layer will fail
+    buildInStore "$storeB"
+}
+
+# Without remounting, we should encounter errors
+expectStderr 1 triggerStaleFileHandle | grepQuiet 'Stale file handle'
+
+# Configure remount-hook and reset OverlayFS
+storeB="$storeB&remount-hook=$PWD/remount.sh"
+remountOverlayfs
+
+# Now it should succeed
+triggerStaleFileHandle
diff --git a/tests/overlay-local-store/stale-file-handle.sh b/tests/overlay-local-store/stale-file-handle.sh
new file mode 100755
index 000000000..5e75628ca
--- /dev/null
+++ b/tests/overlay-local-store/stale-file-handle.sh
@@ -0,0 +1,5 @@
+source common.sh
+
+requireEnvironment
+setupConfig
+execUnshare ./stale-file-handle-inner.sh