diff --git a/src/grpc.rs b/src/grpc.rs
index 5c20ae2..19d9f80 100644
--- a/src/grpc.rs
+++ b/src/grpc.rs
@@ -4,7 +4,7 @@ use std::{
     net::SocketAddr,
     sync::{
         atomic::{AtomicBool, AtomicU64, Ordering},
-        Arc, Mutex,
+        Arc, Mutex, RwLock,
     },
 };
 
@@ -44,19 +44,19 @@ pub(crate) struct ProxyServer {
     current_id: Arc<AtomicU64>,
     clients: Arc<Mutex<ClientMap>>,
     results: Arc<Mutex<HashMap<u64, oneshot::Sender<core_response::Payload>>>>,
-    http_channel: mpsc::UnboundedSender<Key>,
     pub(crate) connected: Arc<AtomicBool>,
     pub(crate) core_version: Arc<Mutex<Option<Version>>>,
     config: Arc<Mutex<Option<Configuration>>>,
+    cookie_key: Arc<RwLock<Option<Key>>>,
     setup_in_progress: Arc<AtomicBool>,
 }
 
 impl ProxyServer {
     #[must_use]
     /// Create new `ProxyServer`.
-    pub(crate) fn new(http_channel: mpsc::UnboundedSender<Key>) -> Self {
+    pub(crate) fn new(cookie_key: Arc<RwLock<Option<Key>>>) -> Self {
         Self {
-            http_channel,
+            cookie_key,
             current_id: Arc::new(AtomicU64::new(1)),
             clients: Arc::new(Mutex::new(HashMap::new())),
             results: Arc::new(Mutex::new(HashMap::new())),
@@ -193,7 +193,7 @@ impl Clone for ProxyServer {
             results: Arc::clone(&self.results),
             connected: Arc::clone(&self.connected),
             core_version: Arc::clone(&self.core_version),
-            http_channel: self.http_channel.clone(),
+            cookie_key: Arc::clone(&self.cookie_key),
             config: Arc::clone(&self.config),
             setup_in_progress: Arc::clone(&self.setup_in_progress),
         }
@@ -252,10 +252,7 @@ impl proxy_server::Proxy for ProxyServer {
                 Key::generate()
             }
         };
-        self.http_channel.send(key).map_err(|err| {
-            error!("Failed to send private cookies key to HTTP server: {err:?}");
-            Status::internal("Failed to send private cookies key to HTTP server")
-        })?;
+        *self.cookie_key.write().unwrap() = Some(key);
 
         let (tx, rx) = mpsc::unbounded_channel();
         self.clients
diff --git a/src/http.rs b/src/http.rs
index 8d165df..c9c5180 100644
--- a/src/http.rs
+++ b/src/http.rs
@@ -3,7 +3,7 @@ use std::{
     fs::read_to_string,
     net::{IpAddr, Ipv4Addr, SocketAddr},
     path::Path,
-    sync::{atomic::Ordering, Arc, LazyLock},
+    sync::{atomic::Ordering, Arc, LazyLock, RwLock},
     time::Duration,
 };
 
@@ -13,6 +13,7 @@ use axum::{
     extract::{ConnectInfo, FromRef, State},
     http::{header::HeaderValue, Request, Response, StatusCode},
     middleware::{self, Next},
+    response::IntoResponse,
     routing::{get, post},
     serve, Json, Router,
 };
@@ -22,7 +23,7 @@ use defguard_version::{server::DefguardVersionLayer, Version};
 use serde::Serialize;
 use tokio::{
     net::TcpListener,
-    sync::{mpsc, oneshot, Mutex},
+    sync::{oneshot, Mutex},
     task::JoinSet,
 };
 use tower_governor::{
@@ -63,7 +64,7 @@ pub(crate) struct AppState {
     pub(crate) grpc_server: ProxyServer,
     pub(crate) remote_mfa_sessions:
         Arc<tokio::sync::Mutex<HashMap<String, oneshot::Sender<String>>>>,
-    key: Key,
+    cookie_key: Arc<RwLock<Option<Key>>>,
     url: Url,
 }
 
@@ -85,7 +86,10 @@ impl AppState {
 
 impl FromRef<AppState> for Key {
     fn from_ref(state: &AppState) -> Self {
-        state.key.clone()
+        let maybe_key = state.cookie_key.read().unwrap().clone();
+        // We return the dummy key only to satisfy the `FromRef` trait, but it is never
+        // used in practice because of the `ensure_configured` middleware.
+        maybe_key.unwrap_or_else(|| Key::from(&[0; 64]))
     }
 }
 
@@ -173,18 +177,44 @@ async fn powered_by_header<B>(mut response: Response<B>) -> Response<B> {
     response
 }
 
+/// Middleware that gates all HTTP endpoints except health checks until the proxy
+/// is fully configured.
+///
+/// The proxy cannot safely handle requests that rely on encrypted cookies
+/// (e.g. OpenID / MFA flows) until it receives the cookie encryption key from
+/// the core. This key is provided asynchronously after the core connects.
+///
+/// Until the key is available, only health check endpoints are served and all
+/// other requests return HTTP 503 (Service Unavailable). Once the key is set,
+/// the middleware becomes a no-op and all routes are enabled.
+async fn ensure_configured(
+    State(state): State<AppState>,
+    request: Request<Body>,
+    next: Next,
+) -> Response<Body> {
+    // Allow healthchecks even before core connects and gives us the cookie key.
+    let path = request.uri().path();
+    if matches!(path, "/api/v1/health" | "/api/v1/health-grpc") {
+        return next.run(request).await;
+    }
+
+    // Block all other requests until cookie key is configured.
+    if state.cookie_key.read().unwrap().is_none() {
+        return StatusCode::SERVICE_UNAVAILABLE.into_response();
+    }
+
+    next.run(request).await
+}
+
 pub async fn run_server(config: Config) -> anyhow::Result<()> {
     info!("Starting Defguard Proxy server");
     debug!("Using config: {config:?}");
 
     let mut tasks = JoinSet::new();
-
-    // Prepare the channel for gRPC -> http server communication.
-    // The channel sends private cookies key once core connects to gRPC.
-    let (tx, mut rx) = mpsc::unbounded_channel::<Key>();
+    let cookie_key = Default::default();
 
     // connect to upstream gRPC server
-    let grpc_server = ProxyServer::new(tx);
+    let grpc_server = ProxyServer::new(Arc::clone(&cookie_key));
 
     let server_clone = grpc_server.clone();
 
@@ -256,15 +286,10 @@ pub async fn run_server(config: Config) -> anyhow::Result<()> {
         }
     });
 
-    // Wait for core to connect to gRPC and send private cookies encryption key.
-    let Some(key) = rx.recv().await else {
-        return Err(anyhow::Error::msg("http channel closed"));
-    };
-
     // build application
     debug!("Setting up API server");
     let shared_state = AppState {
-        key,
+        cookie_key,
         grpc_server,
         remote_mfa_sessions: Arc::new(tokio::sync::Mutex::new(HashMap::new())),
         url: config.url.clone(),
@@ -324,6 +349,10 @@ pub async fn run_server(config: Config) -> anyhow::Result<()> {
                 .route("/info", get(app_info)),
         )
         .fallback_service(get(handle_404))
+        .layer(middleware::from_fn_with_state(
+            shared_state.clone(),
+            ensure_configured,
+        ))
         .layer(middleware::map_response(powered_by_header))
         .layer(middleware::from_fn_with_state(
             shared_state.clone(),