diff --git a/tests/unit/accounts/test_core.py b/tests/unit/accounts/test_core.py
index 94d34ecb1267..24465b78c992 100644
--- a/tests/unit/accounts/test_core.py
+++ b/tests/unit/accounts/test_core.py
@@ -29,9 +29,10 @@
     database_login_factory,
 )
 from warehouse.accounts.tasks import compute_user_metrics
+from warehouse.accounts.utils import UserTokenContext
 from warehouse.oidc.interfaces import SignedClaims
 from warehouse.oidc.models import OIDCPublisher
-from warehouse.oidc.utils import OIDCContext
+from warehouse.oidc.utils import PublisherTokenContext
 from warehouse.rate_limiting import IRateLimiter, RateLimit
 
 from ...common.db.accounts import UserFactory
@@ -45,6 +46,13 @@ def test_with_user(self, db_request):
 
         assert accounts._user(request) is user
 
+    def test_with_user_token_context(self, db_request):
+        user = UserFactory.create()
+        user_ctx = UserTokenContext(user, pretend.stub())
+        request = pretend.stub(identity=user_ctx)
+
+        assert accounts._user(request) is user
+
     def test_without_user_identity(self):
         nonuser = pretend.stub()
         request = pretend.stub(identity=nonuser)
@@ -62,7 +70,7 @@ def test_with_oidc_publisher(self, db_request):
         assert isinstance(publisher, OIDCPublisher)
         claims = SignedClaims({"foo": "bar"})
 
-        request = pretend.stub(identity=OIDCContext(publisher, claims))
+        request = pretend.stub(identity=PublisherTokenContext(publisher, claims))
 
         assert accounts._oidc_publisher(request) is publisher
         assert accounts._oidc_claims(request) is claims
diff --git a/tests/unit/forklift/test_legacy.py b/tests/unit/forklift/test_legacy.py
index 3b798cea6353..463e0cb9cddd 100644
--- a/tests/unit/forklift/test_legacy.py
+++ b/tests/unit/forklift/test_legacy.py
@@ -29,12 +29,13 @@
 from trove_classifiers import classifiers
 from webob.multidict import MultiDict
 
+from warehouse.accounts.utils import UserTokenContext
 from warehouse.admin.flags import AdminFlag, AdminFlagValue
 from warehouse.classifiers.models import Classifier
 from warehouse.forklift import legacy, metadata
 from warehouse.metrics import IMetricsService
 from warehouse.oidc.interfaces import SignedClaims
-from warehouse.oidc.utils import OIDCContext
+from warehouse.oidc.utils import PublisherTokenContext
 from warehouse.packaging.interfaces import IFileStorage, IProjectService
 from warehouse.packaging.models import (
     Dependency,
@@ -945,6 +946,7 @@ def test_upload_escapes_nul_characters(self, pyramid_config, db_request):
 
         assert "\x00" not in db_request.POST["summary"]
 
+    @pytest.mark.parametrize("token_context", [True, False])
     @pytest.mark.parametrize(
         ("digests",),
         [
@@ -973,6 +975,7 @@ def test_successful_upload(
         pyramid_config,
         db_request,
         digests,
+        token_context,
         metrics,
     ):
         monkeypatch.setattr(tempfile, "tempdir", str(tmpdir))
@@ -987,8 +990,13 @@ def test_successful_upload(
 
         filename = f"{project.name}-{release.version}.tar.gz"
 
-        pyramid_config.testing_securitypolicy(identity=user)
         db_request.user = user
+        if token_context:
+            user_context = UserTokenContext(user, pretend.stub())
+            pyramid_config.testing_securitypolicy(identity=user_context)
+        else:
+            pyramid_config.testing_securitypolicy(identity=user)
+
         db_request.user_agent = "warehouse-tests/6.6.6"
 
         content = FieldStorage()
@@ -2975,7 +2983,7 @@ def test_upload_succeeds_creates_release(
         else:
             publisher = GitHubPublisherFactory.create(projects=[project])
             claims = {"sha": "somesha"}
-            identity = OIDCContext(publisher, SignedClaims(claims))
+            identity = PublisherTokenContext(publisher, SignedClaims(claims))
             db_request.oidc_publisher = identity.publisher
             db_request.oidc_claims = identity.claims
 
diff --git a/tests/unit/macaroons/test_caveats.py b/tests/unit/macaroons/test_caveats.py
index 35954ec5dec1..4d9828612ca6 100644
--- a/tests/unit/macaroons/test_caveats.py
+++ b/tests/unit/macaroons/test_caveats.py
@@ -20,6 +20,7 @@
 from pymacaroons import Macaroon
 
 from warehouse.accounts import _oidc_publisher
+from warehouse.accounts.utils import UserTokenContext
 from warehouse.macaroons import caveats
 from warehouse.macaroons.caveats import (
     Caveat,
@@ -36,7 +37,7 @@
     verify,
 )
 from warehouse.macaroons.caveats._core import _CaveatRegistry
-from warehouse.oidc.utils import OIDCContext
+from warehouse.oidc.utils import PublisherTokenContext
 
 from ...common.db.accounts import UserFactory
 from ...common.db.oidc import GitHubPublisherFactory
@@ -280,10 +281,11 @@ def test_verify_invalid_identity(self):
 
     def test_verify_invalid_user_id(self, db_request):
         user = UserFactory.create()
+        user_token_context = UserTokenContext(user, pretend.stub())
 
         caveat = RequestUser(user_id="invalid")
         result = caveat.verify(
-            pretend.stub(identity=user), pretend.stub(), pretend.stub()
+            pretend.stub(identity=user_token_context), pretend.stub(), pretend.stub()
         )
 
         assert result == Failure(
@@ -292,10 +294,11 @@ def test_verify_invalid_user_id(self, db_request):
 
     def test_verify_ok(self, db_request):
         user = UserFactory.create()
+        user_token_context = UserTokenContext(user, pretend.stub())
 
         caveat = RequestUser(user_id=str(user.id))
         result = caveat.verify(
-            pretend.stub(identity=user), pretend.stub(), pretend.stub()
+            pretend.stub(identity=user_token_context), pretend.stub(), pretend.stub()
         )
 
         assert result == Success()
@@ -315,7 +318,7 @@ def test_verify_no_identity(self):
         )
 
     def test_verify_invalid_publisher_id(self, db_request):
-        identity = OIDCContext(GitHubPublisherFactory.create(), None)
+        identity = PublisherTokenContext(GitHubPublisherFactory.create(), None)
         request = pretend.stub(identity=identity)
         request.oidc_publisher = _oidc_publisher(request)
 
@@ -327,7 +330,7 @@ def test_verify_invalid_publisher_id(self, db_request):
         )
 
     def test_verify_invalid_context(self, db_request):
-        identity = OIDCContext(GitHubPublisherFactory.create(), None)
+        identity = PublisherTokenContext(GitHubPublisherFactory.create(), None)
         request = pretend.stub(identity=identity)
         request.oidc_publisher = _oidc_publisher(request)
 
@@ -342,7 +345,9 @@ def test_verify_invalid_project(self, db_request):
 
         # This OIDC publisher is only registered to "foobar", so it should
         # not verify a caveat presented for "foobaz".
-        identity = OIDCContext(GitHubPublisherFactory.create(projects=[foobar]), None)
+        identity = PublisherTokenContext(
+            GitHubPublisherFactory.create(projects=[foobar]), None
+        )
         request = pretend.stub(identity=identity)
         request.oidc_publisher = _oidc_publisher(request)
         caveat = OIDCPublisher(oidc_publisher_id=str(request.oidc_publisher.id))
@@ -356,7 +361,9 @@ def test_verify_ok(self, db_request):
 
         # This OIDC publisher is only registered to "foobar", so it should
         # not verify a caveat presented for "foobaz".
-        identity = OIDCContext(GitHubPublisherFactory.create(projects=[foobar]), None)
+        identity = PublisherTokenContext(
+            GitHubPublisherFactory.create(projects=[foobar]), None
+        )
         request = pretend.stub(identity=identity)
         request.oidc_publisher = _oidc_publisher(request)
         caveat = OIDCPublisher(oidc_publisher_id=str(request.oidc_publisher.id))
diff --git a/tests/unit/macaroons/test_security_policy.py b/tests/unit/macaroons/test_security_policy.py
index 84397ac2bf47..4ce4a2e691b8 100644
--- a/tests/unit/macaroons/test_security_policy.py
+++ b/tests/unit/macaroons/test_security_policy.py
@@ -20,12 +20,13 @@
 from zope.interface.verify import verifyClass
 
 from warehouse.accounts.interfaces import IUserService
+from warehouse.accounts.utils import UserTokenContext
 from warehouse.authnz import Permissions
 from warehouse.macaroons import security_policy
 from warehouse.macaroons.interfaces import IMacaroonService
 from warehouse.macaroons.services import InvalidMacaroonError
 from warehouse.oidc.interfaces import SignedClaims
-from warehouse.oidc.utils import OIDCContext
+from warehouse.oidc.utils import PublisherTokenContext
 
 
 @pytest.mark.parametrize(
@@ -214,7 +215,7 @@ def test_identity_user(self, monkeypatch):
             ),
         )
 
-        assert policy.identity(request) is user
+        assert policy.identity(request) == UserTokenContext(user, macaroon)
         assert extract_http_macaroon.calls == [pretend.call(request)]
         assert request.find_service.calls == [
             pretend.call(IMacaroonService, context=None),
@@ -258,7 +259,7 @@ def test_identity_oidc_publisher(self, monkeypatch):
         identity = policy.identity(request)
         assert identity
         assert identity.publisher is oidc_publisher
-        assert identity == OIDCContext(
+        assert identity == PublisherTokenContext(
             oidc_publisher, SignedClaims(oidc_additional["oidc"])
         )
 
diff --git a/tests/unit/macaroons/test_utils.py b/tests/unit/macaroons/test_utils.py
new file mode 100644
index 000000000000..bbeab50c0667
--- /dev/null
+++ b/tests/unit/macaroons/test_utils.py
@@ -0,0 +1,24 @@
+# Licensed under the Apache License, Version 2.0 (the "License");
+# you may not use this file except in compliance with the License.
+# You may obtain a copy of the License at
+#
+# http://www.apache.org/licenses/LICENSE-2.0
+#
+# Unless required by applicable law or agreed to in writing, software
+# distributed under the License is distributed on an "AS IS" BASIS,
+# WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+# See the License for the specific language governing permissions and
+# limitations under the License.
+
+import pretend
+
+from tests.common.db.accounts import UserFactory
+from warehouse.accounts.utils import UserTokenContext
+from warehouse.utils.security_policy import principals_for
+
+
+def test_usertoken_context_principals(db_request):
+    user = UserFactory.create()
+    assert principals_for(
+        UserTokenContext(user=user, macaroon=pretend.stub())
+    ) == principals_for(user)
diff --git a/tests/unit/oidc/test_utils.py b/tests/unit/oidc/test_utils.py
index 3b51d18bd756..4522eb9b29c4 100644
--- a/tests/unit/oidc/test_utils.py
+++ b/tests/unit/oidc/test_utils.py
@@ -238,7 +238,7 @@ def test_find_publisher_by_issuer_activestate(
 
 def test_oidc_context_principals():
     assert principals_for(
-        utils.OIDCContext(publisher=pretend.stub(id=17), claims=None)
+        utils.PublisherTokenContext(publisher=pretend.stub(id=17), claims=None)
     ) == [
         Authenticated,
         "oidc:17",
diff --git a/tests/unit/utils/test_security_policy.py b/tests/unit/utils/test_security_policy.py
index 0c1c1b0683af..69324b8b8f84 100644
--- a/tests/unit/utils/test_security_policy.py
+++ b/tests/unit/utils/test_security_policy.py
@@ -15,6 +15,8 @@
 from pyramid.interfaces import ISecurityPolicy
 from zope.interface.verify import verifyClass
 
+from tests.common.db.accounts import UserFactory
+from warehouse.accounts.utils import UserTokenContext
 from warehouse.utils import security_policy
 
 
@@ -86,11 +88,24 @@ def test_authenticated_userid_nonuser_identity(self, db_request):
 
         assert policy.authenticated_userid(request) is None
 
-    def test_authenticated_userid(self, monkeypatch):
-        monkeypatch.setattr(security_policy, "User", pretend.stub)
+    def test_authenticated_userid_user_token_context(self, db_request):
+        user = UserFactory.create()
+        user_ctx = UserTokenContext(user, pretend.stub())
+
+        request = pretend.stub(add_finished_callback=lambda *a, **kw: None)
+        subpolicies = [pretend.stub(identity=lambda r: user_ctx)]
+        policy = security_policy.MultiSecurityPolicy(subpolicies)
+
+        assert (
+            policy.authenticated_userid(request)
+            == str(user.id)
+            == str(user_ctx.user.id)
+        )
+
+    def test_authenticated_userid(self, db_request):
+        user = UserFactory.create()
 
         request = pretend.stub(add_finished_callback=lambda *a, **kw: None)
-        user = pretend.stub(id="a fake user")
         subpolicies = [pretend.stub(identity=lambda r: user)]
         policy = security_policy.MultiSecurityPolicy(subpolicies)
 
diff --git a/warehouse/accounts/__init__.py b/warehouse/accounts/__init__.py
index c88cec823f2c..85837cfaa4c4 100644
--- a/warehouse/accounts/__init__.py
+++ b/warehouse/accounts/__init__.py
@@ -32,9 +32,10 @@
     database_login_factory,
 )
 from warehouse.accounts.tasks import compute_user_metrics
+from warehouse.accounts.utils import UserTokenContext
 from warehouse.admin.flags import AdminFlagValue
 from warehouse.macaroons.security_policy import MacaroonSecurityPolicy
-from warehouse.oidc.utils import OIDCContext
+from warehouse.oidc.utils import PublisherTokenContext
 from warehouse.organizations.services import IOrganizationService
 from warehouse.rate_limiting import IRateLimiter, RateLimit
 from warehouse.utils.security_policy import MultiSecurityPolicy
@@ -54,23 +55,29 @@ def _user(request):
     if request.identity is None:
         return None
 
-    if not isinstance(request.identity, User):
+    if isinstance(request.identity, UserTokenContext):
+        # A UserTokenContext signals a user-created API token;
+        # take the underlying user.
+        return request.identity.user
+    elif isinstance(request.identity, User):
+        return request.identity
+    else:
         return None
 
-    return request.identity
-
 
 def _oidc_publisher(request):
     return (
         request.identity.publisher
-        if isinstance(request.identity, OIDCContext)
+        if isinstance(request.identity, PublisherTokenContext)
         else None
     )
 
 
 def _oidc_claims(request):
     return (
-        request.identity.claims if isinstance(request.identity, OIDCContext) else None
+        request.identity.claims
+        if isinstance(request.identity, PublisherTokenContext)
+        else None
     )
 
 
diff --git a/warehouse/accounts/security_policy.py b/warehouse/accounts/security_policy.py
index ab5e15932638..efcb99ec3fa8 100644
--- a/warehouse/accounts/security_policy.py
+++ b/warehouse/accounts/security_policy.py
@@ -171,7 +171,9 @@ def permits(self, request, context, permission):
 
 def _permits_for_user_policy(acl, request, context, permission):
     # It should only be possible for request.identity to be a User object
-    # at this point, and we only a User in these policies.
+    # at this point, and we only allow a User in these policies.
+    # Note that UserTokenContext is not allowed here, since a UserTokenContext
+    # can only appear in an API-token-authenticated request, not a session.
     assert isinstance(request.identity, User)
 
     # Dispatch to our ACL
diff --git a/warehouse/accounts/utils.py b/warehouse/accounts/utils.py
new file mode 100644
index 000000000000..d120945861e2
--- /dev/null
+++ b/warehouse/accounts/utils.py
@@ -0,0 +1,46 @@
+# Licensed under the Apache License, Version 2.0 (the "License");
+# you may not use this file except in compliance with the License.
+# You may obtain a copy of the License at
+#
+# http://www.apache.org/licenses/LICENSE-2.0
+#
+# Unless required by applicable law or agreed to in writing, software
+# distributed under the License is distributed on an "AS IS" BASIS,
+# WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+# See the License for the specific language governing permissions and
+# limitations under the License.
+
+from __future__ import annotations
+
+from dataclasses import dataclass
+from typing import TYPE_CHECKING
+
+if TYPE_CHECKING:
+    from warehouse.accounts.models import User
+    from warehouse.macaroons.models import Macaroon
+
+
+@dataclass
+class UserTokenContext:
+    """
+    This class supports `MacaroonSecurityPolicy` in
+    `warehouse.macaroons.security_policy`.
+
+    It is a wrapper containing both the user associated with an API token
+    authenticated request and its corresponding Macaroon. We use it to smuggle
+    the Macaroon associated to the API token through to a session. `request.identity`
+    in an API token authenticated request should return this type.
+    """
+
+    user: User
+    """
+    The associated user.
+    """
+
+    macaroon: Macaroon
+    """
+    The Macaroon associated to the API token used to authenticate.
+    """
+
+    def __principals__(self) -> list[str]:
+        return self.user.__principals__()
diff --git a/warehouse/macaroons/caveats/__init__.py b/warehouse/macaroons/caveats/__init__.py
index 1b1bcdc06308..9bb112f57488 100644
--- a/warehouse/macaroons/caveats/__init__.py
+++ b/warehouse/macaroons/caveats/__init__.py
@@ -21,7 +21,7 @@
 from pyramid.request import Request
 from pyramid.security import Allowed
 
-from warehouse.accounts.models import User
+from warehouse.accounts.utils import UserTokenContext
 from warehouse.errors import WarehouseDenied
 from warehouse.macaroons.caveats._core import (
     Caveat,
@@ -104,10 +104,10 @@ class RequestUser(Caveat):
     user_id: StrictStr
 
     def verify(self, request: Request, context: Any, permission: str) -> Result:
-        if not isinstance(request.identity, User):
+        if not isinstance(request.identity, UserTokenContext):
             return Failure("token with user restriction without a user")
 
-        if str(request.identity.id) != self.user_id:
+        if str(request.identity.user.id) != self.user_id:
             return Failure("current user does not match user restriction in token")
 
         return Success()
diff --git a/warehouse/macaroons/security_policy.py b/warehouse/macaroons/security_policy.py
index 5190d13cb3c2..0748c1025cc6 100644
--- a/warehouse/macaroons/security_policy.py
+++ b/warehouse/macaroons/security_policy.py
@@ -17,13 +17,14 @@
 from zope.interface import implementer
 
 from warehouse.accounts.interfaces import IUserService
+from warehouse.accounts.utils import UserTokenContext
 from warehouse.authnz import Permissions
 from warehouse.cache.http import add_vary_callback
 from warehouse.errors import WarehouseDenied
 from warehouse.macaroons import InvalidMacaroonError
 from warehouse.macaroons.interfaces import IMacaroonService
 from warehouse.metrics.interfaces import IMetricsService
-from warehouse.oidc.utils import OIDCContext
+from warehouse.oidc.utils import PublisherTokenContext
 from warehouse.utils.security_policy import AuthenticationMethod, principals_for
 
 
@@ -119,9 +120,9 @@ def identity(self, request):
             is_disabled, _ = login_service.is_disabled(dm.user.id)
             if is_disabled:
                 return None
-            return dm.user
+            return UserTokenContext(dm.user, dm)
 
-        return OIDCContext(dm.oidc_publisher, oidc_claims)
+        return PublisherTokenContext(dm.oidc_publisher, oidc_claims)
 
     def remember(self, request, userid, **kw):
         # This is a NO-OP because our Macaroon header policy doesn't allow
diff --git a/warehouse/oidc/utils.py b/warehouse/oidc/utils.py
index 155275748077..3b38f861301e 100644
--- a/warehouse/oidc/utils.py
+++ b/warehouse/oidc/utils.py
@@ -94,7 +94,7 @@ def find_publisher_by_issuer(
 
 
 @dataclass
-class OIDCContext:
+class PublisherTokenContext:
     """
     This class supports `MacaroonSecurityPolicy` in
     `warehouse.macaroons.security_policy`.
diff --git a/warehouse/utils/security_policy.py b/warehouse/utils/security_policy.py
index 25a81860a152..40db36d7aa51 100644
--- a/warehouse/utils/security_policy.py
+++ b/warehouse/utils/security_policy.py
@@ -18,6 +18,7 @@
 from zope.interface import implementer
 
 from warehouse.accounts.models import User
+from warehouse.accounts.utils import UserTokenContext
 
 
 # NOTE: Is there a better place for this to live? It may not even need to exist
@@ -84,6 +85,8 @@ def authenticated_userid(self, request):
             #       more correct pattern before fixing this.
             if isinstance(ident, User):
                 return str(ident.id)
+            elif isinstance(ident, UserTokenContext):
+                return str(ident.user.id)
         return None
 
     def forget(self, request, **kw):