diff --git a/src/libstore/local-overlay-store.cc b/src/libstore/local-overlay-store.cc
index 9e530ed9b..c8464f64d 100644
--- a/src/libstore/local-overlay-store.cc
+++ b/src/libstore/local-overlay-store.cc
@@ -209,13 +209,6 @@ void LocalOverlayStore::optimiseStore()
     }
 }
 
-bool LocalOverlayStore::verifyStore(bool checkContents, RepairFlag repair)
-{
-    if (repair)
-        warn("local-overlay: store does not support --verify --repair");
-    return LocalStore::verifyStore(checkContents, NoRepair);
-}
-
 static RegisterStoreImplementation<LocalOverlayStore, LocalOverlayStoreConfig> regLocalOverlayStore;
 
 }
diff --git a/src/libstore/local-overlay-store.hh b/src/libstore/local-overlay-store.hh
index ef377b7a6..349d9e6ed 100644
--- a/src/libstore/local-overlay-store.hh
+++ b/src/libstore/local-overlay-store.hh
@@ -114,8 +114,6 @@ private:
     void deleteGCPath(const Path & path, uint64_t & bytesFreed) override;
 
     void optimiseStore() override;
-
-    bool verifyStore(bool checkContents, RepairFlag repair) override;
 };
 
 }
diff --git a/tests/overlay-local-store/common.sh b/tests/overlay-local-store/common.sh
index 2b23352ab..6bb5bc391 100644
--- a/tests/overlay-local-store/common.sh
+++ b/tests/overlay-local-store/common.sh
@@ -7,9 +7,13 @@ requireEnvironment () {
   needLocalStore "The test uses --store always so we would just be bypassing the daemon"
 }
 
+addConfig () {
+    echo "$1" >> "$NIX_CONF_DIR/nix.conf"
+}
+
 setupConfig () {
-  echo "require-drop-supplementary-groups = false" >> "$NIX_CONF_DIR"/nix.conf
-  echo "build-users-group = " >> "$NIX_CONF_DIR"/nix.conf
+  addConfig "require-drop-supplementary-groups = false"
+  addConfig "build-users-group = "
 }
 
 
diff --git a/tests/overlay-local-store/verify-inner.sh b/tests/overlay-local-store/verify-inner.sh
index 8f8839302..de40c3d05 100755
--- a/tests/overlay-local-store/verify-inner.sh
+++ b/tests/overlay-local-store/verify-inner.sh
@@ -16,25 +16,51 @@ initLowerStore
 
 mountOverlayfs
 
+
+## Initialise stores for test
+
 # Realise a derivation from the lower store to propagate paths to overlay DB
 nix-store --store "$storeB" --realise $drvPath
 
 # Also ensure dummy file exists in overlay DB
 dummyPath=$(nix-store --store "$storeB" --add ../dummy)
 
+# Add something to the lower store that will not be propagated to overlay DB
+lowerOnlyPath=$(addTextToStore "$storeA" lower-only "Only in lower store")
+
 # Verify should be successful at this point
 nix-store --store "$storeB" --verify --check-contents
 
-# Now delete one of the derivation inputs in the lower store
+# Make a backup so we can repair later
+backupStore="$storeVolume/backup"
+mkdir "$backupStore"
+tar -cC "$storeBRoot" nix | tar -xC "$backupStore"
+
+
+## Deliberately corrupt store paths
+
+# Delete one of the derivation inputs in the lower store
 inputDrvFullPath=$(find "$storeA" -name "*-hermetic-input-1.drv")
 inputDrvPath=${inputDrvFullPath/*\/nix\/store\///nix/store/}
 rm -v "$inputDrvFullPath"
 
-# And truncate the contents of dummy file in lower store
+# Truncate the contents of dummy file in lower store
 find "$storeA" -name "*-dummy" -exec truncate -s 0 {} \;
 
-# Verify should fail with the messages about missing input and modified dummy file
-verifyOutput=$(expectStderr 1 nix-store --store "$storeB" --verify --check-contents --repair)
+# Also truncate the file that only exists in lower store
+truncate -s 0 "$storeA/$lowerOnlyPath"
+
+
+## Now test that verify and repair work as expected
+
+# Verify overlay store without attempting to repair it
+verifyOutput=$(expectStderr 1 nix-store --store "$storeB" --verify --check-contents)
 <<<"$verifyOutput" grepQuiet "path '$inputDrvPath' disappeared, but it still has valid referrers!"
 <<<"$verifyOutput" grepQuiet "path '$dummyPath' was modified! expected hash"
-<<<"$verifyOutput" grepQuiet "store does not support --verify --repair"
+<<<"$verifyOutput" expectStderr 1 grepQuiet "$lowerOnlyPath"  # Expect no error for corrupted lower-only path
+
+# Attempt to repair using backup
+addConfig "substituters = $backupStore"
+repairOutput=$(nix-store --store "$storeB" --verify --check-contents --repair 2>&1)
+<<<"$repairOutput" grepQuiet "copying path '$inputDrvPath'"
+<<<"$repairOutput" grepQuiet "copying path '$dummyPath'"