diff --git a/src/registrar/models/portfolio_invitation.py b/src/registrar/models/portfolio_invitation.py
index a76f0f9f9..68ce69fe3 100644
--- a/src/registrar/models/portfolio_invitation.py
+++ b/src/registrar/models/portfolio_invitation.py
@@ -6,6 +6,7 @@ from django.contrib.auth import get_user_model
 from django.db import models
 
 from django_fsm import FSMField, transition
+from waffle import flag_is_active
 
 from registrar.models.user_portfolio_permission import UserPortfolioPermission
 from .utility.portfolio_helper import UserPortfolioPermissionChoices, UserPortfolioRoleChoices  # type: ignore
@@ -95,3 +96,12 @@ class PortfolioInvitation(TimeStampedModel):
         if self.portfolio_additional_permissions and len(self.portfolio_additional_permissions) > 0:
             user_portfolio_permission.portfolio_additional_permissions = self.portfolio_additional_permissions
         user_portfolio_permission.save()
+
+        # The multiple_portfolios flag ensures that many portfolios can exist per user.
+        # This is (or will be) exposed as a multiselect, which they can choose from.
+        # Without it, we should just add the user on invitation as they'd have no way to select it.
+        # For now, the caller should ensure that this only occurs when no portfolio is selected.
+        # NOTE: Model enforcement of this occurs elsewhere.
+        if not flag_is_active(None, "multiple_portfolios"):
+            user.last_selected_portfolio = user_portfolio_permission.portfolio
+            user.save()
diff --git a/src/registrar/models/user.py b/src/registrar/models/user.py
index 2f173548b..29e0bc90d 100644
--- a/src/registrar/models/user.py
+++ b/src/registrar/models/user.py
@@ -14,7 +14,6 @@ from .transition_domain import TransitionDomain
 from .verified_by_staff import VerifiedByStaff
 from .domain import Domain
 from .domain_request import DomainRequest
-from django.contrib.postgres.fields import ArrayField
 from waffle.decorators import flag_is_active
 
 from phonenumber_field.modelfields import PhoneNumberField  # type: ignore
@@ -378,7 +377,8 @@ class User(AbstractUser):
         for invitation in PortfolioInvitation.objects.filter(
             email__iexact=self.email, status=PortfolioInvitation.PortfolioInvitationStatus.INVITED
         ):
-            if self.last_selected_portfolio is None:
+            only_single_portfolio = not flag_is_active(None, "multiple_portfolios") and self.last_selected_portfolio is None
+            if only_single_portfolio or flag_is_active(None, "multiple_portfolios"):
                 try:
                     invitation.retrieve()
                     invitation.save()