diff --git a/authentik/providers/oauth2/views/token.py b/authentik/providers/oauth2/views/token.py
index c35485253..4e34e1f3b 100644
--- a/authentik/providers/oauth2/views/token.py
+++ b/authentik/providers/oauth2/views/token.py
@@ -12,7 +12,7 @@ from django.utils.timezone import datetime, now
 from django.views import View
 from django.views.decorators.csrf import csrf_exempt
 from guardian.shortcuts import get_anonymous_user
-from jwt import PyJWK, PyJWTError, decode
+from jwt import PyJWK, PyJWT, PyJWTError, decode
 from sentry_sdk.hub import Hub
 from structlog.stdlib import get_logger
 
@@ -306,7 +306,24 @@ class TokenParams:
 
         source: Optional[OAuthSource] = None
         parsed_key: Optional[PyJWK] = None
-        for source in self.provider.jwks_sources.all():
+
+        # Fully decode the JWT without verifying the signature, so we can get access to
+        # the header.
+        # Get the Key ID from the header, and use that to optimise our source query to only find
+        # sources that have a JWK for that Key ID
+        # The Key ID doesn't have a fixed format, but must match between an issued JWT
+        # and whatever is returned by the JWKS endpoint
+        try:
+            decode_unvalidated = PyJWT().decode_complete(
+                assertion, options={"verify_signature": False}
+            )
+        except (PyJWTError, ValueError, TypeError, AttributeError) as exc:
+            LOGGER.warning("failed to parse jwt for kid lookup", exc=exc)
+            raise TokenError("invalid_grant")
+        expected_kid = decode_unvalidated["header"]["kid"]
+        for source in self.provider.jwks_sources.filter(
+            oidc_jwks__keys__contains=[{"kid": expected_kid}]
+        ):
             LOGGER.debug("verifying jwt with source", source=source.slug)
             keys = source.oidc_jwks.get("keys", [])
             for key in keys: