diff --git a/benefits/core/admin.py b/benefits/core/admin.py
index 7daa1f9659..ab874a846e 100644
--- a/benefits/core/admin.py
+++ b/benefits/core/admin.py
@@ -65,14 +65,14 @@ def get_readonly_fields(self, request, obj=None):
             return [
                 "claims_provider",
                 "eligibility_api_url",
-                "eligibility_start_template",
-                "eligibility_unverified_template",
+                "eligibility_start_template_override",
+                "eligibility_unverified_template_override",
                 "help_template",
-                "selection_label_template",
+                "selection_label_template_override",
                 "claims_scheme_override",
                 "enrollment_index_template",
                 "reenrollment_error_template",
-                "enrollment_success_template",
+                "enrollment_success_template_override",
             ]
         else:
             return super().get_readonly_fields(request, obj)
diff --git a/benefits/core/migrations/0029_transitagency_enrollmentflow_optionalfields.py b/benefits/core/migrations/0029_transitagency_enrollmentflow_optionalfields.py
index b7c8411020..0b6cabf8f3 100644
--- a/benefits/core/migrations/0029_transitagency_enrollmentflow_optionalfields.py
+++ b/benefits/core/migrations/0029_transitagency_enrollmentflow_optionalfields.py
@@ -90,6 +90,16 @@ class Migration(migrations.Migration):
             old_name="eligibility_start_template",
             new_name="eligibility_start_template_override",
         ),
+        migrations.RenameField(
+            model_name="enrollmentflow",
+            old_name="eligibility_unverified_template",
+            new_name="eligibility_unverified_template_override",
+        ),
+        migrations.RenameField(
+            model_name="enrollmentflow",
+            old_name="enrollment_index_template",
+            new_name="enrollment_index_template_override",
+        ),
         migrations.RenameField(
             model_name="enrollmentflow",
             old_name="enrollment_success_template",
@@ -121,6 +131,16 @@ class Migration(migrations.Migration):
                 blank=True, help_text="A human readable label, used as the display text in Admin.", null=True
             ),
         ),
+        migrations.AlterField(
+            model_name="enrollmentflow",
+            name="selection_label_template_override",
+            field=models.TextField(
+                blank=True,
+                default=None,
+                help_text="Override the default template that defines the end-user UI for selecting this flow among other options.",  # noqa: E501
+                null=True,
+            ),
+        ),
         migrations.AlterField(
             model_name="enrollmentflow",
             name="eligibility_start_template_override",
@@ -133,21 +153,31 @@ class Migration(migrations.Migration):
         ),
         migrations.AlterField(
             model_name="enrollmentflow",
-            name="enrollment_success_template_override",
+            name="eligibility_unverified_template_override",
             field=models.TextField(
                 blank=True,
-                default="enrollment/success.html",
-                help_text="Override the default template for a successful enrollment associated with the enrollment flow",
+                default=None,
+                help_text="Override the default template that defines the page when a user fails eligibility verification for this flow.",  # noqa: E501
                 null=True,
             ),
         ),
         migrations.AlterField(
             model_name="enrollmentflow",
-            name="selection_label_template_override",
+            name="enrollment_index_template_override",
+            field=models.TextField(
+                blank=True,
+                default=None,
+                help_text="Override the default template for the Eligibility Confirmation page (the index of the enrollment app)",  # noqa: E501
+                null=True,
+            ),
+        ),
+        migrations.AlterField(
+            model_name="enrollmentflow",
+            name="enrollment_success_template_override",
             field=models.TextField(
                 blank=True,
                 default=None,
-                help_text="Override the default template that defines the end-user UI for selecting this flow among other options.",  # noqa
+                help_text="Override the default template for a successful enrollment associated with the enrollment flow",
                 null=True,
             ),
         ),
diff --git a/benefits/core/migrations/local_fixtures.json b/benefits/core/migrations/local_fixtures.json
index eea0847f33..ccbe1217ff 100644
--- a/benefits/core/migrations/local_fixtures.json
+++ b/benefits/core/migrations/local_fixtures.json
@@ -107,8 +107,6 @@
       "system_name": "agency_card",
       "label": "Agency Card",
       "group_id": "group123",
-      "enrollment_index_template": "enrollment/index--agency-card.html",
-      "enrollment_success_template_override": "enrollment/success--cst-agency-card.html",
       "display_order": 4,
       "eligibility_api_url": "http://server:8000/verify",
       "eligibility_api_auth_header": "X-Server-API-Key",
@@ -117,10 +115,7 @@
       "eligibility_api_jwe_cek_enc": "A256CBC-HS512",
       "eligibility_api_jwe_encryption_alg": "RSA-OAEP",
       "eligibility_api_jws_signing_alg": "RS256",
-      "selection_label_template_override": "eligibility/includes/selection-label--cst-agency-card.html",
-      "eligibility_start_template_override": "eligibility/start--cst-agency-card.html",
       "eligibility_form_class": "benefits.eligibility.forms.CSTAgencyCard",
-      "eligibility_unverified_template": "eligibility/unverified--cst-agency-card.html",
       "help_template": "core/includes/help--cst-agency-card.html",
       "supported_enrollment_methods": ["digital", "in_person"],
       "transit_agency": 1
@@ -136,6 +131,7 @@
       "supports_expiration": "True",
       "expiration_days": 5,
       "expiration_reenrollment_days": 3,
+      "enrollment_index_template_override": "enrollment/index--calfresh.html",
       "reenrollment_error_template": "enrollment/reenrollment-error--calfresh.html",
       "display_order": 2,
       "claims_provider": 1,
diff --git a/benefits/core/models.py b/benefits/core/models.py
index f97c9089f8..1d9182071f 100644
--- a/benefits/core/models.py
+++ b/benefits/core/models.py
@@ -378,9 +378,11 @@ class EnrollmentFlow(models.Model):
         blank=True,
         help_text="The fully qualified Python path of a form class used by this flow, e.g. benefits.eligibility.forms.FormClass",  # noqa: E501
     )
-    eligibility_unverified_template = models.TextField(
-        default="eligibility/unverified.html",
-        help_text="Path to a Django template that defines the page when a user fails eligibility verification for this flow.",
+    eligibility_unverified_template_override = models.TextField(
+        help_text="Override the default template that defines the page when a user fails eligibility verification for this flow.",  # noqa: E501
+        blank=True,
+        null=True,
+        default=None,
     )
     help_template = models.TextField(
         null=True,
@@ -404,9 +406,11 @@ class EnrollmentFlow(models.Model):
         blank=True,
         help_text="If the enrollment supports expiration, number of days preceding the expiration date during which a user can re-enroll in the eligibilty",  # noqa: E501
     )
-    enrollment_index_template = models.TextField(
-        default="enrollment/index.html",
-        help_text="Template for the Eligibility Confirmation page (which is the index of the enrollment Django app)",
+    enrollment_index_template_override = models.TextField(
+        help_text="Override the default template for the Eligibility Confirmation page (the index of the enrollment app)",
+        null=True,
+        blank=True,
+        default=None,
     )
     reenrollment_error_template = models.TextField(
         null=True, blank=True, help_text="Template for a re-enrollment error associated with the enrollment flow"
@@ -432,6 +436,13 @@ class Meta:
     def __str__(self):
         return self.label
 
+    @property
+    def agency_card_name(self):
+        if self.uses_claims_verification:
+            return ""
+        else:
+            return f"{self.transit_agency.slug}-agency-card"
+
     @property
     def eligibility_api_auth_key(self):
         if self.eligibility_api_auth_key_secret_name is not None:
@@ -446,11 +457,27 @@ def eligibility_api_public_key_data(self):
 
     @property
     def selection_label_template(self):
-        return self.selection_label_template_override or f"eligibility/includes/selection-label--{self.system_name}.html"
+        prefix = "eligibility/includes/selection-label"
+        if self.uses_claims_verification:
+            return self.selection_label_template_override or f"{prefix}--{self.system_name}.html"
+        else:
+            return self.selection_label_template_override or f"{prefix}--{self.agency_card_name}.html"
 
     @property
     def eligibility_start_template(self):
-        return self.eligibility_start_template_override or f"eligibility/start--{self.system_name}.html"
+        prefix = "eligibility/start"
+        if self.uses_claims_verification:
+            return self.eligibility_start_template_override or f"{prefix}--{self.system_name}.html"
+        else:
+            return self.eligibility_start_template_override or f"{prefix}--{self.agency_card_name}.html"
+
+    @property
+    def eligibility_unverified_template(self):
+        prefix = "eligibility/unverified"
+        if self.uses_claims_verification:
+            return self.eligibility_unverified_template_override or f"{prefix}.html"
+        else:
+            return self.eligibility_unverified_template_override or f"{prefix}--{self.agency_card_name}.html"
 
     @property
     def uses_claims_verification(self):
@@ -468,9 +495,21 @@ def eligibility_verifier(self):
         else:
             return self.eligibility_api_url
 
+    @property
+    def enrollment_index_template(self):
+        prefix = "enrollment/index"
+        if self.uses_claims_verification:
+            return self.enrollment_index_template_override or f"{prefix}.html"
+        else:
+            return self.enrollment_index_template_override or f"{prefix}--agency-card.html"
+
     @property
     def enrollment_success_template(self):
-        return self.enrollment_success_template_override or f"enrollment/success--{self.transit_agency.slug}.html"
+        prefix = "enrollment/success"
+        if self.uses_claims_verification:
+            return self.enrollment_success_template_override or f"{prefix}--{self.transit_agency.slug}.html"
+        else:
+            return self.enrollment_success_template_override or f"{prefix}--{self.agency_card_name}.html"
 
     def eligibility_form_instance(self, *args, **kwargs):
         """Return an instance of this flow's EligibilityForm, or None."""
diff --git a/benefits/eligibility/templates/eligibility/includes/media-item--idcardcheck--start--mst-courtesy-card.html b/benefits/eligibility/templates/eligibility/includes/media-item--idcardcheck--start--mst-agency-card.html
similarity index 100%
rename from benefits/eligibility/templates/eligibility/includes/media-item--idcardcheck--start--mst-courtesy-card.html
rename to benefits/eligibility/templates/eligibility/includes/media-item--idcardcheck--start--mst-agency-card.html
diff --git a/benefits/eligibility/templates/eligibility/includes/media-item--idcardcheck--start--sbmtd-mobility-pass.html b/benefits/eligibility/templates/eligibility/includes/media-item--idcardcheck--start--sbmtd-agency-card.html
similarity index 100%
rename from benefits/eligibility/templates/eligibility/includes/media-item--idcardcheck--start--sbmtd-mobility-pass.html
rename to benefits/eligibility/templates/eligibility/includes/media-item--idcardcheck--start--sbmtd-agency-card.html
diff --git a/benefits/eligibility/templates/eligibility/includes/selection-label--mst-courtesy-card.html b/benefits/eligibility/templates/eligibility/includes/selection-label--mst-agency-card.html
similarity index 100%
rename from benefits/eligibility/templates/eligibility/includes/selection-label--mst-courtesy-card.html
rename to benefits/eligibility/templates/eligibility/includes/selection-label--mst-agency-card.html
diff --git a/benefits/eligibility/templates/eligibility/includes/selection-label--sbmtd-mobility-pass.html b/benefits/eligibility/templates/eligibility/includes/selection-label--sbmtd-agency-card.html
similarity index 100%
rename from benefits/eligibility/templates/eligibility/includes/selection-label--sbmtd-mobility-pass.html
rename to benefits/eligibility/templates/eligibility/includes/selection-label--sbmtd-agency-card.html
diff --git a/benefits/eligibility/templates/eligibility/start--mst-courtesy-card.html b/benefits/eligibility/templates/eligibility/start--mst-agency-card.html
similarity index 96%
rename from benefits/eligibility/templates/eligibility/start--mst-courtesy-card.html
rename to benefits/eligibility/templates/eligibility/start--mst-agency-card.html
index 1cf94ef9e1..5ddfb88b6a 100644
--- a/benefits/eligibility/templates/eligibility/start--mst-courtesy-card.html
+++ b/benefits/eligibility/templates/eligibility/start--mst-agency-card.html
@@ -12,7 +12,7 @@ <h1>{% translate "You selected a Courtesy Card transit benefit." %}</h1>
 {% endblock headline %}
 
 {% block media-item %}
-  {% include "eligibility/includes/media-item--idcardcheck--start--mst-courtesy-card.html" %}
+  {% include "eligibility/includes/media-item--idcardcheck--start--mst-agency-card.html" %}
 {% endblock media-item %}
 
 {% block call-to-action %}
diff --git a/benefits/eligibility/templates/eligibility/start--sbmtd-mobility-pass.html b/benefits/eligibility/templates/eligibility/start--sbmtd-agency-card.html
similarity index 95%
rename from benefits/eligibility/templates/eligibility/start--sbmtd-mobility-pass.html
rename to benefits/eligibility/templates/eligibility/start--sbmtd-agency-card.html
index 0fe01b9e0e..75af35f45d 100644
--- a/benefits/eligibility/templates/eligibility/start--sbmtd-mobility-pass.html
+++ b/benefits/eligibility/templates/eligibility/start--sbmtd-agency-card.html
@@ -12,7 +12,7 @@ <h1>{% translate "You selected a Reduced Fare Mobility ID transit benefit." %}</
 {% endblock headline %}
 
 {% block media-item %}
-    {% include "eligibility/includes/media-item--idcardcheck--start--sbmtd-mobility-pass.html" %}
+    {% include "eligibility/includes/media-item--idcardcheck--start--sbmtd-agency-card.html" %}
 {% endblock media-item %}
 
 {% block call-to-action %}
diff --git a/benefits/eligibility/templates/eligibility/unverified--mst-courtesy-card.html b/benefits/eligibility/templates/eligibility/unverified--mst-agency-card.html
similarity index 100%
rename from benefits/eligibility/templates/eligibility/unverified--mst-courtesy-card.html
rename to benefits/eligibility/templates/eligibility/unverified--mst-agency-card.html
diff --git a/benefits/eligibility/templates/eligibility/unverified--sbmtd-mobility-pass.html b/benefits/eligibility/templates/eligibility/unverified--sbmtd-agency-card.html
similarity index 100%
rename from benefits/eligibility/templates/eligibility/unverified--sbmtd-mobility-pass.html
rename to benefits/eligibility/templates/eligibility/unverified--sbmtd-agency-card.html
diff --git a/benefits/enrollment/templates/enrollment/success--mst-courtesy-card.html b/benefits/enrollment/templates/enrollment/success--mst-agency-card.html
similarity index 100%
rename from benefits/enrollment/templates/enrollment/success--mst-courtesy-card.html
rename to benefits/enrollment/templates/enrollment/success--mst-agency-card.html
diff --git a/benefits/enrollment/templates/enrollment/success--sbmtd-mobility-pass.html b/benefits/enrollment/templates/enrollment/success--sbmtd-agency-card.html
similarity index 100%
rename from benefits/enrollment/templates/enrollment/success--sbmtd-mobility-pass.html
rename to benefits/enrollment/templates/enrollment/success--sbmtd-agency-card.html
diff --git a/tests/pytest/conftest.py b/tests/pytest/conftest.py
index 90e3d38e7c..c38515b724 100644
--- a/tests/pytest/conftest.py
+++ b/tests/pytest/conftest.py
@@ -81,8 +81,10 @@ def model_EnrollmentFlow(model_TransitAgency):
         system_name="test",
         selection_label_template_override="eligibility/includes/selection-label.html",
         eligibility_start_template_override="eligibility/start.html",
+        eligibility_unverified_template_override="eligibility/unverified.html",
         label="Test flow label",
         group_id="group123",
+        enrollment_index_template_override="enrollment/index.html",
         enrollment_success_template_override="enrollment/success.html",
         transit_agency=model_TransitAgency,
     )
diff --git a/tests/pytest/core/test_models.py b/tests/pytest/core/test_models.py
index f6ce89a7e1..b55abbccee 100644
--- a/tests/pytest/core/test_models.py
+++ b/tests/pytest/core/test_models.py
@@ -168,29 +168,23 @@ def test_EnrollmentFlow_supports_expiration(model_EnrollmentFlow_supports_expira
 
 
 @pytest.mark.django_db
-def test_EnrollmentFlow_enrollment_index_template(model_TransitAgency):
-    new_flow = EnrollmentFlow.objects.create(transit_agency=model_TransitAgency)
+def test_EnrollmentFlow_enrollment_index_template(model_EnrollmentFlow_with_scope_and_claim):
+    assert model_EnrollmentFlow_with_scope_and_claim.enrollment_index_template == "enrollment/index.html"
 
-    assert new_flow.enrollment_index_template == "enrollment/index.html"
-
-    new_flow.enrollment_index_template = "test/enrollment.html"
-    new_flow.save()
+    model_EnrollmentFlow_with_scope_and_claim.enrollment_index_template_override = "test/enrollment.html"
+    model_EnrollmentFlow_with_scope_and_claim.save()
 
-    assert new_flow.enrollment_index_template == "test/enrollment.html"
+    assert model_EnrollmentFlow_with_scope_and_claim.enrollment_index_template == "test/enrollment.html"
 
 
 @pytest.mark.django_db
-def test_EnrollmentFlow_enrollment_success_template(model_TransitAgency):
-    new_flow = EnrollmentFlow.objects.create(transit_agency=model_TransitAgency)
-
-    assert new_flow.enrollment_success_template == "enrollment/success.html"
+def test_EnrollmentFlow_enrollment_success_template(model_EnrollmentFlow_with_scope_and_claim):
+    assert model_EnrollmentFlow_with_scope_and_claim.enrollment_success_template == "enrollment/success.html"
 
 
 @pytest.mark.django_db
-def test_EnrollmentFlow_supported_enrollment_methods(model_TransitAgency):
-    new_flow = EnrollmentFlow.objects.create(transit_agency=model_TransitAgency)
-
-    assert new_flow.supported_enrollment_methods == ["digital", "in_person"]
+def test_EnrollmentFlow_supported_enrollment_methods(model_EnrollmentFlow_with_scope_and_claim):
+    assert model_EnrollmentFlow_with_scope_and_claim.supported_enrollment_methods == ["digital", "in_person"]
 
 
 @pytest.mark.django_db
@@ -312,24 +306,76 @@ def test_EnrollmentFlow_with_claims_scheme(model_EnrollmentFlow_with_claims_sche
 
 
 @pytest.mark.django_db
-def test_EnrollmentFlow_template_overrides(model_EnrollmentFlow):
-    assert model_EnrollmentFlow.selection_label_template == model_EnrollmentFlow.selection_label_template_override
-    assert model_EnrollmentFlow.eligibility_start_template == model_EnrollmentFlow.eligibility_start_template_override
-    assert model_EnrollmentFlow.enrollment_success_template == model_EnrollmentFlow.enrollment_success_template_override
+def test_EnrollmentFlow_template_overrides_claims(model_EnrollmentFlow_with_scope_and_claim):
+    assert (
+        model_EnrollmentFlow_with_scope_and_claim.selection_label_template
+        == model_EnrollmentFlow_with_scope_and_claim.selection_label_template_override
+    )
+    assert (
+        model_EnrollmentFlow_with_scope_and_claim.eligibility_start_template
+        == model_EnrollmentFlow_with_scope_and_claim.eligibility_start_template_override
+    )
+    assert (
+        model_EnrollmentFlow_with_scope_and_claim.eligibility_unverified_template
+        == model_EnrollmentFlow_with_scope_and_claim.eligibility_unverified_template_override
+    )
+    assert (
+        model_EnrollmentFlow_with_scope_and_claim.enrollment_index_template
+        == model_EnrollmentFlow_with_scope_and_claim.enrollment_index_template_override
+    )
+    assert (
+        model_EnrollmentFlow_with_scope_and_claim.enrollment_success_template
+        == model_EnrollmentFlow_with_scope_and_claim.enrollment_success_template_override
+    )
 
-    model_EnrollmentFlow.selection_label_template_override = None
-    model_EnrollmentFlow.eligibility_start_template_override = None
-    model_EnrollmentFlow.enrollment_success_template_override = None
-    model_EnrollmentFlow.save()
+    model_EnrollmentFlow_with_scope_and_claim.selection_label_template_override = None
+    model_EnrollmentFlow_with_scope_and_claim.eligibility_start_template_override = None
+    model_EnrollmentFlow_with_scope_and_claim.eligibility_unverified_template_override = None
+    model_EnrollmentFlow_with_scope_and_claim.enrollment_index_template_override = None
+    model_EnrollmentFlow_with_scope_and_claim.enrollment_success_template_override = None
+    model_EnrollmentFlow_with_scope_and_claim.save()
+
+    assert (
+        model_EnrollmentFlow_with_scope_and_claim.selection_label_template
+        == f"eligibility/includes/selection-label--{model_EnrollmentFlow_with_scope_and_claim.system_name}.html"
+    )
+    assert (
+        model_EnrollmentFlow_with_scope_and_claim.eligibility_start_template
+        == f"eligibility/start--{model_EnrollmentFlow_with_scope_and_claim.system_name}.html"
+    )
+    assert model_EnrollmentFlow_with_scope_and_claim.eligibility_unverified_template == "eligibility/unverified.html"
+    assert model_EnrollmentFlow_with_scope_and_claim.enrollment_index_template == "enrollment/index.html"
+    assert (
+        model_EnrollmentFlow_with_scope_and_claim.enrollment_success_template
+        == f"enrollment/success--{model_EnrollmentFlow_with_scope_and_claim.transit_agency.slug}.html"
+    )
 
+
+@pytest.mark.django_db
+def test_EnrollmentFlow_template_overrides_eligibility_api(model_EnrollmentFlow_with_eligibility_api):
+    model_EnrollmentFlow_with_eligibility_api.selection_label_template_override = None
+    model_EnrollmentFlow_with_eligibility_api.eligibility_start_template_override = None
+    model_EnrollmentFlow_with_eligibility_api.eligibility_unverified_template_override = None
+    model_EnrollmentFlow_with_eligibility_api.enrollment_index_template_override = None
+    model_EnrollmentFlow_with_eligibility_api.enrollment_success_template_override = None
+    model_EnrollmentFlow_with_eligibility_api.save()
+
+    assert (
+        model_EnrollmentFlow_with_eligibility_api.selection_label_template
+        == f"eligibility/includes/selection-label--{model_EnrollmentFlow_with_eligibility_api.agency_card_name}.html"
+    )
+    assert (
+        model_EnrollmentFlow_with_eligibility_api.eligibility_start_template
+        == f"eligibility/start--{model_EnrollmentFlow_with_eligibility_api.agency_card_name}.html"
+    )
     assert (
-        model_EnrollmentFlow.selection_label_template
-        == f"eligibility/includes/selection-label--{model_EnrollmentFlow.system_name}.html"
+        model_EnrollmentFlow_with_eligibility_api.eligibility_unverified_template
+        == f"eligibility/unverified--{model_EnrollmentFlow_with_eligibility_api.agency_card_name}.html"
     )
-    assert model_EnrollmentFlow.eligibility_start_template == f"eligibility/start--{model_EnrollmentFlow.system_name}.html"
+    assert model_EnrollmentFlow_with_eligibility_api.enrollment_index_template == "enrollment/index--agency-card.html"
     assert (
-        model_EnrollmentFlow.enrollment_success_template
-        == f"enrollment/success--{model_EnrollmentFlow.transit_agency.slug}.html"
+        model_EnrollmentFlow_with_eligibility_api.enrollment_success_template
+        == f"enrollment/success--{model_EnrollmentFlow_with_eligibility_api.agency_card_name}.html"
     )