diff --git a/api/src/adapters/oauth/login_gov/mock_login_gov_oauth_client.py b/api/src/adapters/oauth/login_gov/mock_login_gov_oauth_client.py
index e437b8a5a2..a47e1793df 100644
--- a/api/src/adapters/oauth/login_gov/mock_login_gov_oauth_client.py
+++ b/api/src/adapters/oauth/login_gov/mock_login_gov_oauth_client.py
@@ -7,15 +7,29 @@ class MockLoginGovOauthClient(BaseOauthClient):
     def __init__(self) -> None:
         self.responses: dict[str, OauthTokenResponse] = {}
 
+        # Used to control testing of retry behavior for Login.gov token lookup calls
+        self.retries: dict[str, int] = {}
+
     def add_token_response(self, code: str, response: OauthTokenResponse) -> None:
         self.responses[code] = response
 
     def get_token(self, request: OauthTokenRequest) -> OauthTokenResponse:
-        response = self.responses.get(request.code, None)
+        retries = self.retries.get(request.code)
+        # if we don't have retries enabled on the mock, behave as usual
+        if retries is not None:
+            self.retries[request.code] = retries - 1
+        # retries would be one the last time through, as we've reduced it to zero but retries accounts for the data before that
+        if retries is None or retries == 1:
+            response = self.responses.get(request.code, None)
+
+            if response is None:
+                response = OauthTokenResponse(
+                    error="error", error_description="default mock error description"
+                )
 
-        if response is None:
-            response = OauthTokenResponse(
-                error="error", error_description="default mock error description"
-            )
+            return response
 
-        return response
+        # if we did turn on retries on the mock, do retry stuff
+        return OauthTokenResponse(
+            error="error", error_description="mock oauth token error description"
+        )
diff --git a/api/src/services/users/login_gov_callback_handler.py b/api/src/services/users/login_gov_callback_handler.py
index 9c50549841..a2bf0ce99d 100644
--- a/api/src/services/users/login_gov_callback_handler.py
+++ b/api/src/services/users/login_gov_callback_handler.py
@@ -161,15 +161,26 @@ def handle_login_gov_token(
     # call the token endpoint (make a client)
     # https://developers.login.gov/oidc/token/
     client = get_login_gov_client()
-    response = client.get_token(
-        OauthTokenRequest(
-            code=login_gov_data.code, client_assertion=get_login_gov_client_assertion()
+    limit = 3
+    tries = 0
+    while tries < limit:
+        tries += 1
+        response = client.get_token(
+            OauthTokenRequest(
+                code=login_gov_data.code, client_assertion=get_login_gov_client_assertion()
+            )
         )
-    )
 
-    # If this request failed, we'll assume we're the issue and 500
-    if response.is_error_response():
-        raise_flask_error(500, response.error_description)
+        # If this request failed, we'll assume we're the issue and 500
+        if response.is_error_response():
+            if tries == limit:
+                raise_flask_error(500, response.error_description)
+            else:
+                logger.info(
+                    "Retrying call to Login.gov after receiving error",
+                    extra={"tries": tries, "limit": limit},
+                )
+                continue
 
     # Process the token response from login.gov
     # which will create/update a user in the DB
diff --git a/api/tests/src/api/users/test_user_route_login.py b/api/tests/src/api/users/test_user_route_login.py
index af476e716c..e4bde5b2f0 100644
--- a/api/tests/src/api/users/test_user_route_login.py
+++ b/api/tests/src/api/users/test_user_route_login.py
@@ -690,3 +690,98 @@ def test_agency_user_without_piv_succeeds_when_not_required(
     resp_json = resp.get_json()
     assert resp_json["message"] == "success"
     assert resp_json["token"] is not None
+
+
+def test_user_callback_retries_success(
+    client, db_session, enable_factory_create, mock_oauth_client, private_rsa_key
+):
+    # Create state so the callback gets past the check
+    login_gov_state = LoginGovStateFactory.create()
+
+    code = str(uuid.uuid4())
+    id_token = create_jwt(
+        user_id="bob-xyz",
+        nonce=str(login_gov_state.nonce),
+        private_key=private_rsa_key,
+    )
+    mock_oauth_client.add_token_response(
+        code,
+        OauthTokenResponse(
+            id_token=id_token, access_token="fake_token", token_type="Bearer", expires_in=300
+        ),
+    )
+    mock_oauth_client.retries[code] = 3
+
+    resp = client.get(
+        f"/v1/users/login/callback?state={login_gov_state.login_gov_state_id}&code={code}",
+        follow_redirects=True,
+    )
+
+    assert resp.status_code == 200
+    resp_json = resp.get_json()
+    assert resp_json["is_user_new"] == "0"
+    assert resp_json["message"] == "success"
+    assert resp_json["token"] is not None
+
+    user_token_session = parse_jwt_for_user(resp_json["token"], db_session)
+    assert user_token_session.expires_at > datetime_util.utcnow()
+    assert user_token_session.is_valid is True
+
+    # Make sure the external user record is created with expected IDs
+    external_user = (
+        db_session.query(LinkExternalUser)
+        .filter(
+            LinkExternalUser.user_id == user_token_session.user_id,
+            LinkExternalUser.external_user_id == "bob-xyz",
+        )
+        .one_or_none()
+    )
+    assert external_user is not None
+
+    # Make sure the login gov state was deleted
+    db_state = (
+        db_session.query(LoginGovState)
+        .filter(LoginGovState.login_gov_state_id == login_gov_state.login_gov_state_id)
+        .one_or_none()
+    )
+    assert db_state is None
+
+
+def test_user_callback_retries_failure(
+    client, db_session, enable_factory_create, mock_oauth_client, private_rsa_key
+):
+    # Create state so the callback gets past the check
+    login_gov_state = LoginGovStateFactory.create()
+
+    code = str(uuid.uuid4())
+    id_token = create_jwt(
+        user_id="bob-xyz",
+        nonce=str(login_gov_state.nonce),
+        private_key=private_rsa_key,
+    )
+    mock_oauth_client.add_token_response(
+        code,
+        OauthTokenResponse(
+            id_token=id_token, access_token="fake_token", token_type="Bearer", expires_in=300
+        ),
+    )
+    mock_oauth_client.retries[code] = 4
+
+    resp = client.get(
+        f"/v1/users/login/callback?state={login_gov_state.login_gov_state_id}&code={code}",
+        follow_redirects=True,
+    )
+
+    assert resp.status_code == 200
+    resp_json = resp.get_json()
+
+    assert resp_json["message"] == "error"
+    assert resp_json["error_description"] == "internal error"
+
+    # History contains each redirect, we redirected just once
+    assert len(resp.history) == 1
+    redirect = resp.history[0]
+
+    assert redirect.status_code == 302
+    redirect_url = urllib.parse.urlparse(redirect.headers["Location"])
+    assert redirect_url.path == "/v1/users/login/result"