diff --git a/server.go b/server.go
index c289d46..189aa97 100644
--- a/server.go
+++ b/server.go
@@ -251,7 +251,7 @@ func New(sink *olog.Sink, opts ...ServerOption) *Server {
 		sink:            sink,
 		agentsDir:       agentsDir,
 		agentStore:      NewFlatDirStore(agentsDir, 0644),
-		promptStore:     NewFlatDirStore(agent.DefaultPromptsDir(), 0444),
+		promptStore:     store.NewFlatDirUnion(agent.PromptsDirs(), 0444),
 		memStore:        NewFlatDirStore(memDir, 0644),
 		toolStore:       NewToolStore(),
 		utilStore:       NewUtilStore(),
diff --git a/store/store.go b/store/store.go
index 4d17618..bb80689 100644
--- a/store/store.go
+++ b/store/store.go
@@ -111,6 +111,66 @@ func NewFlatDir(dir string, perm os.FileMode) Store {
 	}
 }
 
+// NewFlatDirUnion returns a read-only Store that merges multiple directories.
+// Files are deduplicated by name; the first directory containing a name wins.
+func NewFlatDirUnion(dirs []string, perm os.FileMode) Store {
+	notBlocking := func(context.Context, string) ([]byte, error) {
+		return nil, fmt.Errorf("blocking read not supported")
+	}
+
+	resolve := func(name string) (string, error) {
+		for _, dir := range dirs {
+			p := filepath.Join(dir, name)
+			if _, err := os.Stat(p); err == nil {
+				return p, nil
+			}
+		}
+		return "", fmt.Errorf("%s: not found", name)
+	}
+
+	return &storeConfig{
+		StatFn: func(name string) (os.FileInfo, error) {
+			p, err := resolve(name)
+			if err != nil {
+				return nil, err
+			}
+			return os.Stat(p)
+		},
+		ListFn: func() ([]os.DirEntry, error) {
+			seen := make(map[string]bool)
+			var result []os.DirEntry
+			for _, dir := range dirs {
+				entries, err := os.ReadDir(dir)
+				if err != nil {
+					continue
+				}
+				for _, e := range entries {
+					if !seen[e.Name()] {
+						seen[e.Name()] = true
+						result = append(result, e)
+					}
+				}
+			}
+			return result, nil
+		},
+		OpenFn: func(name string) (StoreEntry, error) {
+			p, err := resolve(name)
+			if err != nil {
+				return nil, err
+			}
+			return &EntryConfig{
+				StatFn:         func() (os.FileInfo, error) { return os.Stat(p) },
+				ReadFn:         func() ([]byte, error) { return os.ReadFile(p) },
+				WriteFn:        func([]byte) error { return fmt.Errorf("%s: read-only", name) },
+				BlockingReadFn: notBlocking,
+			}, nil
+		},
+		CreateFn: func(string) error { return fmt.Errorf("read-only store") },
+		DeleteFn: func(string) error { return fmt.Errorf("read-only store") },
+		RenameFn: func(string, string) error { return fmt.Errorf("read-only store") },
+	}
+}
+
 // SyntheticFileInfo implements os.FileInfo for entries with no backing file.
 type SyntheticFileInfo struct {
 	Name_  string