diff --git a/src/dstack/_internal/proxy/gateway/app.py b/src/dstack/_internal/proxy/gateway/app.py
index 6627e9e3f..7bd690eab 100644
--- a/src/dstack/_internal/proxy/gateway/app.py
+++ b/src/dstack/_internal/proxy/gateway/app.py
@@ -1,6 +1,8 @@
 """FastAPI app running on a gateway."""
 
-from contextlib import asynccontextmanager
+import asyncio
+import random
+from contextlib import asynccontextmanager, suppress
 from pathlib import Path
 from typing import Optional
 
@@ -30,11 +32,16 @@
 from dstack._internal.proxy.gateway.services.stats import StatsCollector
 from dstack._internal.proxy.lib.routers.model_proxy import router as model_proxy_router
 from dstack._internal.utils.common import run_async
+from dstack._internal.utils.logging import get_logger
 from dstack.version import __version__
 
 STATE_FILE = DSTACK_DIR_ON_GATEWAY / "state-v2.json"
 LEGACY_STATE_FILE = DSTACK_DIR_ON_GATEWAY / "state.json"
 LEGACY_KEYS_DIR = Path("~/.ssh/projects").expanduser().resolve()
+# `certbot renew` only renews certificates close to expiry. Twice a day matches the
+# schedule of the timer that certbot's own packages install.
+CERT_RENEWAL_INTERVAL = 12 * 3600
+logger = get_logger(__name__)
 
 
 @asynccontextmanager
@@ -45,12 +52,29 @@ async def lifespan(app: FastAPI):
     service_conn_pool = await injector.get_service_connection_pool()
     await run_async(nginx.write_global_conf)
     await apply_all(repo, nginx, service_conn_pool)
+    renewal_task = asyncio.create_task(renew_certificates_periodically(nginx))
 
     yield
 
+    renewal_task.cancel()
+    with suppress(asyncio.CancelledError):
+        await renewal_task
     await service_conn_pool.remove_all()
 
 
+async def renew_certificates_periodically(nginx: Nginx) -> None:
+    # Gateways on some backends, e.g. Kubernetes, have no system timer that runs
+    # `certbot renew`, so the gateway renews its certificates itself. The random
+    # first delay spreads renewals of many gateways over the interval.
+    await asyncio.sleep(random.uniform(0, CERT_RENEWAL_INTERVAL))
+    while True:
+        try:
+            await nginx.renew_certificates()
+        except Exception as e:
+            logger.warning("Failed to renew TLS certificates: %r", e)
+        await asyncio.sleep(CERT_RENEWAL_INTERVAL)
+
+
 def make_app(repo: Optional[GatewayProxyRepo] = None, nginx: Optional[Nginx] = None) -> FastAPI:
     if repo is None:
         migrate_from_state_v1(
diff --git a/src/dstack/_internal/proxy/gateway/services/nginx.py b/src/dstack/_internal/proxy/gateway/services/nginx.py
index df71594f5..9a76a5502 100644
--- a/src/dstack/_internal/proxy/gateway/services/nginx.py
+++ b/src/dstack/_internal/proxy/gateway/services/nginx.py
@@ -18,6 +18,7 @@
 
 CERTBOT_TIMEOUT = 40
 CERTBOT_2ND_TIMEOUT = 5
+CERTBOT_RENEW_TIMEOUT = 600
 NGINX_DIR = Path("/etc/nginx")
 logger = get_logger(__name__)
 
@@ -109,6 +110,29 @@ async def unregister(self, service: models.Service) -> None:
             await run_async(self.reload)
         logger.info("Unregistered domain %s", domain)
 
+    async def renew_certificates(self) -> None:
+        """Renew the certificates that are due."""
+        # Holding the lock keeps this certbot run from colliding with `run_certbot`
+        async with self._lock:
+            await run_async(self.run_certbot_renew)
+
+    @staticmethod
+    def run_certbot_renew() -> None:
+        # Certbot renews each certificate with the ACME server that issued it.
+        # The deploy hook reloads nginx only if some certificate was renewed.
+        cmd = ["sudo", "timeout", "--kill-after", str(CERTBOT_2ND_TIMEOUT)]
+        cmd += [str(CERTBOT_RENEW_TIMEOUT), "certbot", "renew"]
+        cmd += ["--non-interactive", "--quiet", "--no-random-sleep-on-renew"]
+        cmd += ["--deploy-hook", "systemctl reload nginx.service"]
+        r = subprocess.run(
+            cmd,
+            capture_output=True,
+            timeout=CERTBOT_RENEW_TIMEOUT + CERTBOT_2ND_TIMEOUT + 1,  # shouldn't happen
+        )
+        if r.returncode != 0:
+            msg = r.stderr.decode().strip().replace("\n", " ")
+            raise UnexpectedProxyError(f"Error renewing TLS certificates: {msg}")
+
     @staticmethod
     def reload() -> None:
         cmd = ["sudo", "systemctl", "reload", "nginx.service"]
diff --git a/src/tests/_internal/proxy/gateway/services/test_nginx.py b/src/tests/_internal/proxy/gateway/services/test_nginx.py
new file mode 100644
index 000000000..85abe3a85
--- /dev/null
+++ b/src/tests/_internal/proxy/gateway/services/test_nginx.py
@@ -0,0 +1,40 @@
+import asyncio
+from pathlib import Path
+from unittest.mock import Mock, patch
+
+import pytest
+
+from dstack._internal.proxy.gateway.services.nginx import Nginx
+from dstack._internal.proxy.lib.errors import UnexpectedProxyError
+
+SUBPROCESS_RUN = "dstack._internal.proxy.gateway.services.nginx.subprocess.run"
+
+
+class TestRunCertbotRenew:
+    def test_renews_and_reloads_nginx_on_deploy(self) -> None:
+        with patch(SUBPROCESS_RUN) as run:
+            run.return_value = Mock(returncode=0, stderr=b"")
+            Nginx.run_certbot_renew()
+        cmd = run.call_args.args[0]
+        assert cmd[0] == "sudo"
+        assert cmd[cmd.index("certbot") + 1] == "renew"
+        assert "--non-interactive" in cmd
+        assert cmd[cmd.index("--deploy-hook") + 1] == "systemctl reload nginx.service"
+
+    def test_raises_on_failure(self) -> None:
+        with patch(SUBPROCESS_RUN) as run:
+            run.return_value = Mock(returncode=1, stderr=b"Failed to renew\nexample.com\n")
+            with pytest.raises(UnexpectedProxyError, match="Failed to renew example.com"):
+                Nginx.run_certbot_renew()
+
+
+@pytest.mark.asyncio
+async def test_renew_certificates_waits_for_registration(tmp_path: Path) -> None:
+    nginx = Nginx(nginx_dir=tmp_path)
+    with patch.object(Nginx, "run_certbot_renew") as run_certbot_renew:
+        async with nginx._lock:  # e.g. a service registration is running certbot
+            task = asyncio.create_task(nginx.renew_certificates())
+            await asyncio.sleep(0.1)
+            run_certbot_renew.assert_not_called()
+        await task
+        run_certbot_renew.assert_called_once()
diff --git a/src/tests/_internal/proxy/gateway/test_app.py b/src/tests/_internal/proxy/gateway/test_app.py
index 335be84fa..685586731 100644
--- a/src/tests/_internal/proxy/gateway/test_app.py
+++ b/src/tests/_internal/proxy/gateway/test_app.py
@@ -1,8 +1,14 @@
+import asyncio
 from pathlib import Path
+from unittest.mock import AsyncMock, Mock, patch
 
 import pytest
 
-from dstack._internal.proxy.gateway.app import lifespan, make_app
+from dstack._internal.proxy.gateway.app import (
+    lifespan,
+    make_app,
+    renew_certificates_periodically,
+)
 from dstack._internal.proxy.gateway.models import ModelEntrypoint
 from dstack._internal.proxy.gateway.repo.repo import GatewayProxyRepo
 from dstack._internal.proxy.gateway.services.nginx import Nginx
@@ -32,3 +38,14 @@ async def test_lifespan(tmp_path: Path, system_mocks: Mocks) -> None:
         assert system_mocks.open_conn.call_count == 1
         assert system_mocks.close_conn.call_count == 0
     assert system_mocks.close_conn.call_count == 1
+
+
+@pytest.mark.asyncio
+async def test_renews_certificates_periodically_despite_errors() -> None:
+    nginx = Mock(renew_certificates=AsyncMock(side_effect=[RuntimeError("certbot failed"), None]))
+    # The first delay, then one after each of the two renewals; stop at the third
+    sleep = AsyncMock(side_effect=[None, None, asyncio.CancelledError()])
+    with patch("dstack._internal.proxy.gateway.app.asyncio.sleep", sleep):
+        with pytest.raises(asyncio.CancelledError):
+            await renew_certificates_periodically(nginx)
+    assert nginx.renew_certificates.await_count == 2