diff --git a/python/ray/_private/authentication/authentication_constants.py b/python/ray/_private/authentication/authentication_constants.py
index 77b090af7afe..eabb96e7bba8 100644
--- a/python/ray/_private/authentication/authentication_constants.py
+++ b/python/ray/_private/authentication/authentication_constants.py
@@ -24,6 +24,7 @@
 
 AUTHORIZATION_HEADER_NAME = "authorization"
 AUTHORIZATION_BEARER_PREFIX = "Bearer "
+RAY_AUTHORIZATION_HEADER_NAME = "x-ray-authorization"
 
 AUTHENTICATION_TOKEN_COOKIE_NAME = "ray-authentication-token"
 AUTHENTICATION_TOKEN_COOKIE_MAX_AGE = 30 * 24 * 60 * 60  # 30 days
diff --git a/python/ray/_private/authentication/http_token_authentication.py b/python/ray/_private/authentication/http_token_authentication.py
index 58a49f5048eb..5c4b5114b4b9 100644
--- a/python/ray/_private/authentication/http_token_authentication.py
+++ b/python/ray/_private/authentication/http_token_authentication.py
@@ -43,12 +43,20 @@ async def token_auth_middleware(request, handler):
         ):
             return await handler(request)
 
-        # Check Authorization header first (for API clients)
+        # Try to get authentication token from multiple sources (in priority order):
+        # 1. Standard "Authorization" header (for API clients, SDKs)
+        # 2. Fallback "X-Ray-Authorization" header (for proxies and KubeRay)
+        # 3. Cookie (for web dashboard sessions)
+
         auth_header = request.headers.get(
             authentication_constants.AUTHORIZATION_HEADER_NAME, ""
         )
 
-        # If no Authorization header, check cookie (for web dashboard)
+        if not auth_header:
+            auth_header = request.headers.get(
+                authentication_constants.RAY_AUTHORIZATION_HEADER_NAME, ""
+            )
+
         if not auth_header:
             token = request.cookies.get(
                 authentication_constants.AUTHENTICATION_TOKEN_COOKIE_NAME
diff --git a/python/ray/dashboard/tests/test_dashboard_auth.py b/python/ray/dashboard/tests/test_dashboard_auth.py
index 1df2a65d96f0..8ec89a46cfe8 100644
--- a/python/ray/dashboard/tests/test_dashboard_auth.py
+++ b/python/ray/dashboard/tests/test_dashboard_auth.py
@@ -50,6 +50,54 @@ def test_dashboard_request_requires_auth_invalid_token(setup_cluster_with_token_
     assert response.status_code == 403
 
 
+def test_dashboard_request_with_ray_auth_header(setup_cluster_with_token_auth):
+    """Test that requests succeed with valid token in X-Ray-Authorization header."""
+
+    cluster_info = setup_cluster_with_token_auth
+    headers = {"X-Ray-Authorization": f"Bearer {cluster_info['token']}"}
+
+    response = requests.get(
+        f"{cluster_info['dashboard_url']}/api/component_activities",
+        headers=headers,
+    )
+
+    assert response.status_code == 200
+
+
+def test_authorization_header_takes_precedence(setup_cluster_with_token_auth):
+    """Test that standard Authorization header takes precedence over X-Ray-Authorization."""
+
+    cluster_info = setup_cluster_with_token_auth
+
+    # Provide both headers: valid token in Authorization, invalid in X-Ray-Authorization
+    headers = {
+        "Authorization": f"Bearer {cluster_info['token']}",
+        "X-Ray-Authorization": "Bearer invalid_token_000000000000000000000000",
+    }
+
+    # Should succeed because Authorization header takes precedence
+    response = requests.get(
+        f"{cluster_info['dashboard_url']}/api/component_activities",
+        headers=headers,
+    )
+
+    assert response.status_code == 200
+
+    # Now test with invalid Authorization but valid X-Ray-Authorization
+    headers = {
+        "Authorization": "Bearer invalid_token_000000000000000000000000",
+        "X-Ray-Authorization": f"Bearer {cluster_info['token']}",
+    }
+
+    # Should fail because Authorization header takes precedence (even though it's invalid)
+    response = requests.get(
+        f"{cluster_info['dashboard_url']}/api/component_activities",
+        headers=headers,
+    )
+
+    assert response.status_code == 403
+
+
 def test_dashboard_auth_disabled(setup_cluster_without_token_auth):
     """Test that auth is not enforced when AUTH_MODE is disabled."""