diff --git a/plugins/content/local/store.go b/plugins/content/local/store.go
index 30ecb156b522..794c82c25e3b 100644
--- a/plugins/content/local/store.go
+++ b/plugins/content/local/store.go
@@ -68,8 +68,9 @@ type store struct {
 	ls                 LabelStore
 	integritySupported bool
 
-	locksMu sync.Mutex
-	locks   map[string]*lock
+	locksMu              sync.Mutex
+	locks                map[string]*lock
+	ensureIngestRootOnce func() error
 }
 
 // NewStore returns a local content store
@@ -83,18 +84,16 @@ func NewStore(root string) (content.Store, error) {
 // require labels and should use `NewStore`. `NewLabeledStore` is primarily
 // useful for tests or standalone implementations.
 func NewLabeledStore(root string, ls LabelStore) (content.Store, error) {
-	if err := os.MkdirAll(filepath.Join(root, "ingest"), 0777); err != nil {
-		return nil, err
-	}
-
 	supported, _ := fsverity.IsSupported(root)
 
-	return &store{
+	s := &store{
 		root:               root,
 		ls:                 ls,
 		integritySupported: supported,
 		locks:              map[string]*lock{},
-	}, nil
+	}
+	s.ensureIngestRootOnce = sync.OnceValue(s.ensureIngestRoot)
+	return s, nil
 }
 
 func (s *store) Info(ctx context.Context, dgst digest.Digest) (content.Info, error) {
@@ -301,6 +300,9 @@ func (s *store) Status(ctx context.Context, ref string) (content.Status, error)
 func (s *store) ListStatuses(ctx context.Context, fs ...string) ([]content.Status, error) {
 	fp, err := os.Open(filepath.Join(s.root, "ingest"))
 	if err != nil {
+		if os.IsNotExist(err) {
+			return nil, nil
+		}
 		return nil, err
 	}
 	defer fp.Close()
@@ -350,6 +352,9 @@ func (s *store) ListStatuses(ctx context.Context, fs ...string) ([]content.Statu
 func (s *store) WalkStatusRefs(ctx context.Context, fn func(string) error) error {
 	fp, err := os.Open(filepath.Join(s.root, "ingest"))
 	if err != nil {
+		if os.IsNotExist(err) {
+			return nil
+		}
 		return err
 	}
 	defer fp.Close()
@@ -536,6 +541,11 @@ func (s *store) writer(ctx context.Context, ref string, total int64, expected di
 	)
 
 	foundValidIngest := false
+
+	if err := s.ensureIngestRootOnce(); err != nil {
+		return nil, err
+	}
+
 	// ensure that the ingest path has been created.
 	if err := os.Mkdir(path, 0755); err != nil {
 		if !os.IsExist(err) {
@@ -646,6 +656,10 @@ func (s *store) ingestPaths(ref string) (string, string, string) {
 	return fp, rp, dp
 }
 
+func (s *store) ensureIngestRoot() error {
+	return os.MkdirAll(filepath.Join(s.root, "ingest"), 0777)
+}
+
 func readFileString(path string) (string, error) {
 	p, err := os.ReadFile(path)
 	return string(p), err
diff --git a/plugins/content/local/store_test.go b/plugins/content/local/store_test.go
index 6e42190944f8..827c5e97f982 100644
--- a/plugins/content/local/store_test.go
+++ b/plugins/content/local/store_test.go
@@ -108,10 +108,6 @@ func TestContentWriter(t *testing.T) {
 	defer cleanup()
 	defer testutil.DumpDirOnFailure(t, tmpdir)
 
-	if _, err := os.Stat(filepath.Join(tmpdir, "ingest")); os.IsNotExist(err) {
-		t.Fatal("ingest dir should be created", err)
-	}
-
 	cw, err := cs.Writer(ctx, content.WithRef("myref"))
 	if err != nil {
 		t.Fatal(err)
@@ -120,6 +116,10 @@ func TestContentWriter(t *testing.T) {
 		t.Fatal(err)
 	}
 
+	if _, err := os.Stat(filepath.Join(tmpdir, "ingest")); os.IsNotExist(err) {
+		t.Fatal("ingest dir should be created", err)
+	}
+
 	// reopen, so we can test things
 	cw, err = cs.Writer(ctx, content.WithRef("myref"))
 	if err != nil {