diff --git a/app/models/filter.rb b/app/models/filter.rb
index d96ae6e9175..1c4ff7b4d69 100644
--- a/app/models/filter.rb
+++ b/app/models/filter.rb
@@ -165,7 +165,22 @@ def enforce_inherited_taxonomies
   def inherit_taxonomies!
     self.organization_ids = role.organization_ids if resource_taxable_by_organization?
     self.location_ids = role.location_ids if resource_taxable_by_location?
-    build_taxonomy_search
+    build_taxonomy_search_from_ids
+  end
+
+  def build_taxonomy_search_from_ids
+    orgs = build_taxonomy_search_string_from_ids('organization')
+    locs = build_taxonomy_search_string_from_ids('location')
+
+    taxonomies = [orgs, locs].reject { |t| t.blank? }
+    self.taxonomy_search = taxonomies.join(' and ').presence
+  end
+
+  def build_taxonomy_search_string_from_ids(name)
+    return '' unless send("resource_taxable_by_#{name}?")
+    relation = send("#{name}_ids")
+    return '' if relation.empty?
+    parenthesize("#{name}_id ^ (#{relation.join(',')})")
   end
 
   private
diff --git a/db/migrate/20241105143353_regenerate_taxonomy_search_for_filters_with_override_false.rb b/db/migrate/20241105143353_regenerate_taxonomy_search_for_filters_with_override_false.rb
new file mode 100644
index 00000000000..9b3931ffeb4
--- /dev/null
+++ b/db/migrate/20241105143353_regenerate_taxonomy_search_for_filters_with_override_false.rb
@@ -0,0 +1,10 @@
+class RegenerateTaxonomySearchForFiltersWithOverrideFalse < ActiveRecord::Migration[6.1]
+  def change
+    filters = Filter.where(role_id: Role.where(origin: nil).or(Role.where(builtin: 2))).where(override: false).where(taxonomy_search: nil)
+
+    filters.each do |filter|
+      filter.build_taxonomy_search_from_ids
+      filter.update_column(:taxonomy_search, filter.taxonomy_search)
+    end
+  end
+end
diff --git a/test/models/filter_test.rb b/test/models/filter_test.rb
index ade9b53f924..bca1965a77d 100644
--- a/test/models/filter_test.rb
+++ b/test/models/filter_test.rb
@@ -245,8 +245,17 @@ class FilterTest < ActiveSupport::TestCase
 
   test 'saving nilifies empty taxonomy search' do
     f = FactoryBot.build(:filter, :resource_type => 'Domain')
-    f.role = FactoryBot.build(:role, :organizations => [FactoryBot.build(:organization)])
+    f.role = FactoryBot.build(:role)
     f.save
     assert_nil f.taxonomy_search
   end
+
+  test 'creating a filter inherits taxonomies from the role' do
+    f = FactoryBot.create(:filter, :resource_type => 'Domain')
+    organization_test = FactoryBot.create(:organization)
+    location_test = FactoryBot.create(:location)
+    f.role = FactoryBot.create(:role, :organizations => [organization_test], :locations => [location_test])
+    f.save
+    assert_equal f.taxonomy_search(), "(organization_id ^ (#{organization_test.id})) and (location_id ^ (#{location_test.id}))"
+  end
 end
diff --git a/webpack/assets/javascripts/react_app/routes/FiltersForm/FiltersForm.js b/webpack/assets/javascripts/react_app/routes/FiltersForm/FiltersForm.js
index 765b71a91a2..65c2fa598a4 100644
--- a/webpack/assets/javascripts/react_app/routes/FiltersForm/FiltersForm.js
+++ b/webpack/assets/javascripts/react_app/routes/FiltersForm/FiltersForm.js
@@ -1,4 +1,4 @@
-import React, { useState } from 'react';
+import React, { useState, useEffect, useMemo } from 'react';
 import PropTypes from 'prop-types';
 import { useDispatch } from 'react-redux';
 import {
@@ -39,6 +39,17 @@ export const FiltersForm = ({ roleName, roleId, isNew, data, history }) => {
     show_organizations: showOrgs = false,
     show_locations: showLocations = false,
   } = type;
+
+  const isTaxonomySearch = useMemo(
+    () => chosenOrgs.length || chosenLocations.length,
+    [chosenOrgs.length, chosenLocations.length]
+  );
+
+  useEffect(() => {
+    if (isTaxonomySearch) {
+      setIsUnlimited(false);
+    }
+  }, [isTaxonomySearch]);
   const dispatch = useDispatch();
   const [autocompleteQuery, setAutocompleteQuery] = useState(data.search || '');
   const submit = async () => {
@@ -46,7 +57,8 @@ export const FiltersForm = ({ roleName, roleId, isNew, data, history }) => {
       filter: {
         role_id: role,
         search: isUnlimited ? null : autocompleteQuery,
-        unlimited: isUnlimited,
+        unlimited:
+          isUnlimited || (!autocompleteQuery.length && !isTaxonomySearch),
         override: isOverride,
         permission_ids: chosenPermissions,
         organization_ids: chosenOrgs,
@@ -163,8 +175,20 @@ export const FiltersForm = ({ roleName, roleId, isNew, data, history }) => {
           defaultLocations={data.locations}
         />
       )}
+
       {isGranular ? (
         <>
+          {!!isTaxonomySearch && (
+            <>
+              <Alert
+                ouiaId="taxonomy-search-alert"
+                variant="info"
+                title={__(
+                  "The filter is scoped to the selected organizations and locations, therefore can't be unlimited"
+                )}
+              />
+            </>
+          )}
           <FormGroup
             label={__('Unlimited?')}
             labelIcon={
@@ -190,11 +214,12 @@ export const FiltersForm = ({ roleName, roleId, isNew, data, history }) => {
           >
             <Checkbox
               ouiaId="unlimited-checkbox"
-              isChecked={isUnlimited}
+              isChecked={isTaxonomySearch ? isUnlimited : false}
               onChange={checked => {
                 setAutocompleteQuery('');
                 setIsUnlimited(checked);
               }}
+              isDisabled={isTaxonomySearch}
               aria-label="is unlimited"
               id="unlimited-check"
               name="unlimited"
diff --git a/webpack/assets/javascripts/react_app/routes/FiltersForm/NewFiltersFormPage.js b/webpack/assets/javascripts/react_app/routes/FiltersForm/NewFiltersFormPage.js
index e059164ba1c..500f952b218 100644
--- a/webpack/assets/javascripts/react_app/routes/FiltersForm/NewFiltersFormPage.js
+++ b/webpack/assets/javascripts/react_app/routes/FiltersForm/NewFiltersFormPage.js
@@ -9,7 +9,7 @@ import { FiltersForm } from './FiltersForm';
 const NewFiltersFormPage = ({ location: { search }, history }) => {
   const { role_id: urlRoleId } = URI.parseQuery(search);
   const {
-    response: { name: roleName, id: roleId },
+    response: { name: roleName, id: roleId, locations, organizations },
   } = useAPI('get', `/api/v2/roles/${urlRoleId}`);
   const breadcrumbOptions = {
     breadcrumbItems: [
@@ -29,7 +29,7 @@ const NewFiltersFormPage = ({ location: { search }, history }) => {
           isNew
           roleName={roleName || ''}
           roleId={urlRoleId}
-          data={{}}
+          data={{ locations, organizations }}
           history={history}
         />
       ) : (