diff --git a/.gitignore b/.gitignore
index c06ec47a78..c98c2698b3 100644
--- a/.gitignore
+++ b/.gitignore
@@ -95,6 +95,7 @@ experimenter/experimenter/reporting/reporting-ui/assets/
 .tmontmp
 experimenter/coverage_html_report/
 experimenter/tests/integration/test-reports/
+experimenter/tests/integration/nimbus/fixtures/targeting_configs.json
 junit.xml
 **/coverage_report/
 
diff --git a/Makefile b/Makefile
index 1e3941fd3c..622852a1ac 100644
--- a/Makefile
+++ b/Makefile
@@ -60,6 +60,7 @@ LOAD_COUNTRIES = python manage.py loaddata ./experimenter/base/fixtures/countrie
 LOAD_LOCALES = python manage.py loaddata ./experimenter/base/fixtures/locales.json
 LOAD_LANGUAGES = python manage.py loaddata ./experimenter/base/fixtures/languages.json
 LOAD_FEATURES = python manage.py load_feature_configs
+GENERATE_TARGETING_CONFIGS = python manage.py generate_targeting_configs
 LOAD_DUMMY_EXPERIMENTS = [[ -z $$SKIP_DUMMY ]] && python manage.py load_dummy_experiments || python manage.py load_dummy_tags
 
 JETSTREAM_CONFIG_URL = https://github.com/mozilla/metric-hub/archive/main.zip
@@ -226,7 +227,7 @@ bash: build_dev cirrus_build
 refresh: kill build_dev cirrus_build compose_build refresh_db  ## Rebuild all containers and the database
 
 refresh_db:  # Rebuild the database
-	$(COMPOSE_RUN) -e SKIP_DUMMY=$$SKIP_DUMMY experimenter bash -c '$(WAIT_FOR_DB) $(PYTHON_MIGRATE)&&$(LOAD_LOCALES)&&$(LOAD_COUNTRIES)&&$(LOAD_LANGUAGES)&&$(LOAD_FEATURES)&&$(LOAD_DUMMY_EXPERIMENTS)'
+	$(COMPOSE_RUN) -e SKIP_DUMMY=$$SKIP_DUMMY experimenter bash -c '$(WAIT_FOR_DB) $(PYTHON_MIGRATE)&&$(LOAD_LOCALES)&&$(LOAD_COUNTRIES)&&$(LOAD_LANGUAGES)&&$(LOAD_FEATURES)&&$(GENERATE_TARGETING_CONFIGS)&&$(LOAD_DUMMY_EXPERIMENTS)'
 
 dependabot_approve:
 	echo "Install and configure the Github CLI https://github.com/cli/cli"
diff --git a/experimenter/experimenter/base/management/commands/generate_targeting_configs.py b/experimenter/experimenter/base/management/commands/generate_targeting_configs.py
new file mode 100644
index 0000000000..d5f0efb7cd
--- /dev/null
+++ b/experimenter/experimenter/base/management/commands/generate_targeting_configs.py
@@ -0,0 +1,40 @@
+import json
+import logging
+from pathlib import Path
+
+from django.core.management.base import BaseCommand
+
+from experimenter.targeting.constants import NimbusTargetingConfig
+
+logger = logging.getLogger()
+
+OUTPUT_PATH = (
+    Path(__file__).resolve().parents[4]
+    / "tests"
+    / "integration"
+    / "nimbus"
+    / "fixtures"
+    / "targeting_configs.json"
+)
+
+
+class Command(BaseCommand):
+    help = "Generate targeting configs JSON for integration tests"
+
+    def handle(self, *args, **options):
+        configs = [
+            {
+                "label": config.name,
+                "value": config.slug,
+                "applicationValues": list(config.application_choice_names),
+                "description": config.description,
+                "stickyRequired": config.sticky_required,
+                "isFirstRunRequired": config.is_first_run_required,
+            }
+            for config in NimbusTargetingConfig.targeting_configs
+        ]
+
+        OUTPUT_PATH.parent.mkdir(parents=True, exist_ok=True)
+        OUTPUT_PATH.write_text(json.dumps(configs, indent=2) + "\n")
+
+        logger.info(f"Generated {len(configs)} targeting configs to {OUTPUT_PATH}")
diff --git a/experimenter/experimenter/targeting/tests/test_generate_targeting_configs.py b/experimenter/experimenter/targeting/tests/test_generate_targeting_configs.py
new file mode 100644
index 0000000000..e591bdd30d
--- /dev/null
+++ b/experimenter/experimenter/targeting/tests/test_generate_targeting_configs.py
@@ -0,0 +1,43 @@
+import json
+from unittest.mock import patch
+
+from django.core.management import call_command
+from django.test import TestCase
+
+from experimenter.targeting.constants import NimbusTargetingConfig
+
+
+class TestGenerateTargetingConfigsCommand(TestCase):
+    def test_generates_json_file(self):
+        with patch(
+            "experimenter.base.management.commands.generate_targeting_configs.OUTPUT_PATH"
+        ) as mock_path:
+            mock_path.parent.mkdir.return_value = None
+
+            call_command("generate_targeting_configs")
+
+            mock_path.parent.mkdir.assert_called_once_with(parents=True, exist_ok=True)
+            mock_path.write_text.assert_called_once()
+
+            written_json = mock_path.write_text.call_args[0][0]
+            configs = json.loads(written_json)
+
+            self.assertEqual(len(configs), len(NimbusTargetingConfig.targeting_configs))
+
+            for config in configs:
+                self.assertIn("label", config)
+                self.assertIn("value", config)
+                self.assertIn("applicationValues", config)
+                self.assertIn("description", config)
+                self.assertIn("stickyRequired", config)
+                self.assertIn("isFirstRunRequired", config)
+
+            first = configs[0]
+            source = NimbusTargetingConfig.targeting_configs[0]
+            self.assertEqual(first["label"], source.name)
+            self.assertEqual(first["value"], source.slug)
+            self.assertEqual(
+                first["applicationValues"], list(source.application_choice_names)
+            )
+            self.assertEqual(first["stickyRequired"], source.sticky_required)
+            self.assertEqual(first["isFirstRunRequired"], source.is_first_run_required)
diff --git a/experimenter/tests/integration/nimbus/utils/helpers.py b/experimenter/tests/integration/nimbus/utils/helpers.py
index d878a32a78..3721c63e5d 100755
--- a/experimenter/tests/integration/nimbus/utils/helpers.py
+++ b/experimenter/tests/integration/nimbus/utils/helpers.py
@@ -2,6 +2,7 @@
 import os
 import time
 from functools import cache
+from pathlib import Path
 
 import requests
 
@@ -11,6 +12,9 @@
 
 LOAD_DATA_RETRIES = 60
 LOAD_DATA_RETRY_DELAY = 1.0
+TARGETING_CONFIGS_PATH = (
+    Path(__file__).resolve().parents[1] / "fixtures" / "targeting_configs.json"
+)
 
 
 def load_graphql_data(query):
@@ -142,10 +146,10 @@ def load_config_data():
 
 
 def load_targeting_configs(app=BaseExperimentApplications.FIREFOX_DESKTOP.value):
-    config_data = load_config_data()
+    targeting_configs = json.loads(TARGETING_CONFIGS_PATH.read_text())
     return [
         item["value"]
-        for item in config_data["targetingConfigs"]
+        for item in targeting_configs
         if (
             BaseExperimentApplications.FIREFOX_DESKTOP.value in app
             and BaseExperimentApplications.FIREFOX_DESKTOP.value