diff --git a/backend/app/core/auth.py b/backend/app/core/auth.py
index d72b65091..4716b5c11 100644
--- a/backend/app/core/auth.py
+++ b/backend/app/core/auth.py
@@ -1,7 +1,10 @@
 from __future__ import annotations
 
+import logging
+import os
 import secrets
 from datetime import datetime, timedelta
+from pathlib import Path
 from typing import Annotated
 
 import jwt
@@ -19,13 +22,67 @@ from backend.app.models.api_key import APIKey
 from backend.app.models.settings import Settings
 from backend.app.models.user import User
 
+logger = logging.getLogger(__name__)
+
 # Password hashing
 # Use pbkdf2_sha256 instead of bcrypt to avoid 72-byte limit and passlib initialization issues
 # pbkdf2_sha256 is a secure password hashing algorithm without bcrypt's limitations
 pwd_context = CryptContext(schemes=["pbkdf2_sha256"], deprecated="auto")
 
+
+def _get_jwt_secret() -> str:
+    """Get the JWT secret key from environment, file, or generate a new one.
+
+    Priority:
+    1. JWT_SECRET_KEY environment variable
+    2. .jwt_secret file in data directory
+    3. Generate new random secret and save to file
+
+    Returns:
+        The JWT secret key
+    """
+    # 1. Check environment variable first
+    env_secret = os.environ.get("JWT_SECRET_KEY")
+    if env_secret:
+        logger.info("Using JWT secret from JWT_SECRET_KEY environment variable")
+        return env_secret
+
+    # 2. Check for secret file in data directory
+    data_dir = Path(os.environ.get("BAMBUDDY_DATA_DIR", "/app/data"))
+    secret_file = data_dir / ".jwt_secret"
+
+    if secret_file.exists():
+        try:
+            secret = secret_file.read_text().strip()
+            if secret and len(secret) >= 32:
+                logger.info("Using JWT secret from %s", secret_file)
+                return secret
+        except Exception as e:
+            logger.warning("Failed to read JWT secret file: %s", e)
+
+    # 3. Generate new random secret
+    new_secret = secrets.token_urlsafe(64)
+
+    # Try to save it
+    try:
+        data_dir.mkdir(parents=True, exist_ok=True)
+        secret_file.write_text(new_secret)
+        # Restrict permissions (owner read/write only)
+        secret_file.chmod(0o600)
+        logger.info("Generated new JWT secret and saved to %s", secret_file)
+    except Exception as e:
+        logger.warning(
+            "Could not save JWT secret to file (%s). "
+            "Secret will be regenerated on restart, invalidating existing tokens. "
+            "Set JWT_SECRET_KEY environment variable for persistence.",
+            e,
+        )
+
+    return new_secret
+
+
 # JWT settings
-SECRET_KEY = "bambuddy-secret-key-change-in-production"  # TODO: Move to settings/env
+SECRET_KEY = _get_jwt_secret()
 ALGORITHM = "HS256"
 ACCESS_TOKEN_EXPIRE_MINUTES = 60 * 24 * 7  # 7 days
 
diff --git a/backend/app/main.py b/backend/app/main.py
index e36d5cc89..9c7bb34ae 100644
--- a/backend/app/main.py
+++ b/backend/app/main.py
@@ -2537,6 +2537,121 @@ app = FastAPI(
     lifespan=lifespan,
 )
 
+
+# =============================================================================
+# Authentication Middleware - Secures ALL API routes by default
+# =============================================================================
+# Public routes that don't require authentication even when auth is enabled
+PUBLIC_API_ROUTES = {
+    # Auth routes needed before login
+    "/api/v1/auth/status",
+    "/api/v1/auth/login",
+    # Version check for updates (no sensitive data)
+    "/api/v1/updates/version",
+}
+
+# Route prefixes that are public (for routes with dynamic segments)
+PUBLIC_API_PREFIXES = [
+    # WebSocket connections handle their own auth
+    "/api/v1/ws",
+]
+
+
+@app.middleware("http")
+async def auth_middleware(request, call_next):
+    """Enforce authentication on all API routes when auth is enabled.
+
+    This middleware provides defense-in-depth by checking auth at the API gateway level,
+    regardless of whether individual routes have auth dependencies.
+    """
+    from starlette.responses import JSONResponse
+
+    path = request.url.path
+
+    # Only apply to API routes
+    if not path.startswith("/api/"):
+        return await call_next(request)
+
+    # Allow public routes
+    if path in PUBLIC_API_ROUTES:
+        return await call_next(request)
+
+    # Allow public prefixes
+    for prefix in PUBLIC_API_PREFIXES:
+        if path.startswith(prefix):
+            return await call_next(request)
+
+    # Check if auth is enabled
+    try:
+        async with async_session() as db:
+            from backend.app.core.auth import is_auth_enabled
+
+            auth_enabled = await is_auth_enabled(db)
+
+        if not auth_enabled:
+            # Auth disabled, allow all requests
+            return await call_next(request)
+    except Exception:
+        # If we can't check auth status, allow request (fail open for DB issues)
+        return await call_next(request)
+
+    # Auth is enabled - require valid token
+    auth_header = request.headers.get("Authorization")
+    x_api_key = request.headers.get("X-API-Key")
+
+    # Check for API key auth first
+    if x_api_key or (auth_header and auth_header.startswith("Bearer bb_")):
+        # API key authentication - let the request through to be validated by route handler
+        # API keys are validated per-route since they have different permission levels
+        return await call_next(request)
+
+    # Check for JWT auth
+    if not auth_header or not auth_header.startswith("Bearer "):
+        return JSONResponse(
+            status_code=401,
+            content={"detail": "Authentication required"},
+            headers={"WWW-Authenticate": "Bearer"},
+        )
+
+    # Validate JWT token
+    try:
+        import jwt
+
+        from backend.app.core.auth import ALGORITHM, SECRET_KEY
+
+        token = auth_header.replace("Bearer ", "")
+        payload = jwt.decode(token, SECRET_KEY, algorithms=[ALGORITHM])
+        username = payload.get("sub")
+        if not username:
+            raise ValueError("No username in token")
+
+        # Verify user exists and is active
+        async with async_session() as db:
+            from backend.app.core.auth import get_user_by_username
+
+            user = await get_user_by_username(db, username)
+            if not user or not user.is_active:
+                return JSONResponse(
+                    status_code=401,
+                    content={"detail": "User not found or inactive"},
+                    headers={"WWW-Authenticate": "Bearer"},
+                )
+    except jwt.ExpiredSignatureError:
+        return JSONResponse(
+            status_code=401,
+            content={"detail": "Token has expired"},
+            headers={"WWW-Authenticate": "Bearer"},
+        )
+    except (jwt.InvalidTokenError, ValueError, Exception):
+        return JSONResponse(
+            status_code=401,
+            content={"detail": "Invalid token"},
+            headers={"WWW-Authenticate": "Bearer"},
+        )
+
+    return await call_next(request)
+
+
 # API routes
 app.include_router(auth.router, prefix=app_settings.api_prefix)
 app.include_router(users.router, prefix=app_settings.api_prefix)
diff --git a/backend/tests/conftest.py b/backend/tests/conftest.py
index e56ee875b..40f487405 100644
--- a/backend/tests/conftest.py
+++ b/backend/tests/conftest.py
@@ -117,10 +117,11 @@ async def async_client(test_engine, db_session) -> AsyncGenerator[AsyncClient, N
     async def mock_init_printer_connections(db):
         pass  # No-op - don't connect to real printers
 
-    # Also patch the module-level async_session used by services and auth
+    # Also patch the module-level async_session used by services, auth, and middleware
     with (
         patch("backend.app.core.database.async_session", test_async_session),
         patch("backend.app.core.auth.async_session", test_async_session),
+        patch("backend.app.main.async_session", test_async_session),
         patch("backend.app.main.init_printer_connections", mock_init_printer_connections),
     ):
         # Seed default groups for tests that need them
diff --git a/backend/tests/integration/test_ownership_permissions.py b/backend/tests/integration/test_ownership_permissions.py
index 2d0063f76..9b01a0d57 100644
--- a/backend/tests/integration/test_ownership_permissions.py
+++ b/backend/tests/integration/test_ownership_permissions.py
@@ -700,7 +700,10 @@ class TestUserItemsCountAndDeletion(TestOwnershipPermissionsSetup):
         assert response.status_code == 204
 
         # Verify archive still exists but is now ownerless
-        archive_response = await async_client.get(f"/api/v1/archives/{archive_id}")
+        archive_response = await async_client.get(
+            f"/api/v1/archives/{archive_id}",
+            headers={"Authorization": f"Bearer {auth_setup['admin_token']}"},
+        )
         assert archive_response.status_code == 200
         assert archive_response.json()["created_by_id"] is None
 
@@ -736,5 +739,8 @@ class TestUserItemsCountAndDeletion(TestOwnershipPermissionsSetup):
         assert response.status_code == 204
 
         # Verify archive was deleted
-        archive_response = await async_client.get(f"/api/v1/archives/{archive_id}")
+        archive_response = await async_client.get(
+            f"/api/v1/archives/{archive_id}",
+            headers={"Authorization": f"Bearer {auth_setup['admin_token']}"},
+        )
         assert archive_response.status_code == 404