diff --git a/components/runners/ambient-runner/ambient_runner/_grpc_client.py b/components/runners/ambient-runner/ambient_runner/_grpc_client.py
index 2f7782af2..a5cacb98b 100644
--- a/components/runners/ambient-runner/ambient_runner/_grpc_client.py
+++ b/components/runners/ambient-runner/ambient_runner/_grpc_client.py
@@ -11,10 +11,11 @@
 from pathlib import Path
 from typing import Optional
 
+import grpc
 from cryptography.hazmat.primitives import hashes, serialization
 from cryptography.hazmat.primitives.asymmetric import padding
 
-import grpc
+from ambient_runner.platform.utils import set_bot_token
 
 logger = logging.getLogger(__name__)
 
@@ -95,6 +96,7 @@ def _fetch_token_from_cp(cp_token_url: str, public_key_pem: str, session_id: str
             if not token:
                 raise RuntimeError("CP /token response missing 'token' field")
             logger.info("[GRPC CLIENT] Fetched fresh API token from CP token endpoint")
+            set_bot_token(token)
             return token
         except urllib.error.HTTPError as e:
             resp_body = ""
diff --git a/components/runners/ambient-runner/ambient_runner/platform/utils.py b/components/runners/ambient-runner/ambient_runner/platform/utils.py
index 5f3393d22..6820c5623 100644
--- a/components/runners/ambient-runner/ambient_runner/platform/utils.py
+++ b/components/runners/ambient-runner/ambient_runner/platform/utils.py
@@ -23,14 +23,27 @@
 # Kubelet automatically refreshes this file when the Secret is updated.
 _BOT_TOKEN_FILE = Path("/var/run/secrets/ambient/bot-token")
 
+# In-process cache for the token fetched from the CP token endpoint.
+# Set once at startup by _grpc_client.py after a successful CP token fetch.
+_cp_fetched_token: str = ""
+
+
+def set_bot_token(token: str) -> None:
+    """Store a token fetched from the CP token endpoint for use by get_bot_token()."""
+    global _cp_fetched_token
+    _cp_fetched_token = token.strip()
+
 
 def get_bot_token() -> str:
-    """Return the current BOT_TOKEN, preferring the file mount over env var.
+    """Return the current BOT_TOKEN.
 
-    The operator mounts the runner-token Secret as a file so kubelet refreshes
-    it automatically when the token is rotated. Falls back to the BOT_TOKEN
-    env var for backward-compatibility with local / non-Kubernetes runs.
+    Priority:
+    1. Token fetched from CP token endpoint (set via set_bot_token()).
+    2. File mount at _BOT_TOKEN_FILE (kubelet-refreshed Secret).
+    3. BOT_TOKEN env var (local / non-Kubernetes fallback).
     """
+    if _cp_fetched_token:
+        return _cp_fetched_token
     try:
         if _BOT_TOKEN_FILE.exists():
             return _BOT_TOKEN_FILE.read_text().strip()
diff --git a/components/runners/ambient-runner/tests/test_grpc_client.py b/components/runners/ambient-runner/tests/test_grpc_client.py
index baf379fd2..de6734307 100644
--- a/components/runners/ambient-runner/tests/test_grpc_client.py
+++ b/components/runners/ambient-runner/tests/test_grpc_client.py
@@ -200,6 +200,51 @@ def test_raises_on_missing_token_field(self):
                     )
 
 
+class TestSetBotTokenIntegration:
+    def test_get_bot_token_returns_cp_fetched_token_after_successful_fetch(self):
+        import ambient_runner.platform.utils as utils
+        utils._cp_fetched_token = ""
+
+        _, _, public_pem = generate_keypair()
+        mock_resp = MagicMock()
+        mock_resp.read.return_value = json.dumps({"token": "oidc-token-for-api-calls"}).encode()
+        mock_resp.__enter__ = MagicMock(return_value=mock_resp)
+        mock_resp.__exit__ = MagicMock(return_value=False)
+
+        assert utils.get_bot_token() == "", "get_bot_token() must be empty before any CP fetch"
+
+        with patch("urllib.request.urlopen", return_value=mock_resp):
+            _fetch_token_from_cp("http://cp.svc:8080/token", public_pem, "session-12345678")
+
+        assert utils.get_bot_token() == "oidc-token-for-api-calls", (
+            "get_bot_token() must return the CP-fetched token so backend API credential "
+            "calls are authenticated — regression for HTTP 401 on credential refresh"
+        )
+        utils._cp_fetched_token = ""
+
+    def test_fetch_from_cp_calls_set_bot_token(self):
+        from cryptography.hazmat.primitives.asymmetric import rsa as _rsa
+        private_key = _rsa.generate_private_key(public_exponent=65537, key_size=2048)
+        public_pem = private_key.public_key().public_bytes(
+            encoding=serialization.Encoding.PEM,
+            format=serialization.PublicFormat.SubjectPublicKeyInfo,
+        ).decode()
+
+        mock_resp = MagicMock()
+        mock_resp.read.return_value = json.dumps({"token": "oidc-api-token-abc"}).encode()
+        mock_resp.__enter__ = MagicMock(return_value=mock_resp)
+        mock_resp.__exit__ = MagicMock(return_value=False)
+
+        import ambient_runner.platform.utils as utils
+        utils._cp_fetched_token = ""
+
+        with patch("urllib.request.urlopen", return_value=mock_resp):
+            _fetch_token_from_cp("http://cp.svc:8080/token", public_pem, "session-12345678")
+
+        assert utils.get_bot_token() == "oidc-api-token-abc"
+        utils._cp_fetched_token = ""
+
+
 class TestFromEnvIntegration:
     def test_uses_encrypted_session_id_when_cp_token_url_set(self):
         _, _, public_pem = generate_keypair()