diff --git a/fluxcd/assets/configuration/spec.yaml b/fluxcd/assets/configuration/spec.yaml
index af748939d282d..ac695fc3d4101 100644
--- a/fluxcd/assets/configuration/spec.yaml
+++ b/fluxcd/assets/configuration/spec.yaml
@@ -2,6 +2,12 @@ name: fluxcd
 fleet_configurable: true
 files:
 - name: fluxcd.yaml
+  discovery:
+    strategies:
+    - template: discovery/openmetrics_from_named_ports
+      overrides:
+        port_names:
+        - http-prom
   options:
   - template: init_config
     options:
@@ -15,3 +21,22 @@ files:
         for Flux custom resources (Flux 2.1+).
       value:
         type: string
+- name: auto_conf.yaml
+  options:
+  - template: ad_identifiers
+    overrides:
+      value.example:
+      - helm-controller
+      - image-automation-controller
+      - image-reflector-controller
+      - kustomize-controller
+      - notification-controller
+      - source-controller
+  - template: auto_conf/cel_selector
+    overrides:
+      cel_selector.example:
+        containers:
+        # Narrow down matching containers since the controller names are generic
+        # and don't identify the container as being part of FluxCD.
+        - container.image.reference.contains("fluxcd/")
+  - template: auto_conf/discovery
diff --git a/fluxcd/changelog.d/24510.added b/fluxcd/changelog.d/24510.added
new file mode 100644
index 0000000000000..1455667b0b73f
--- /dev/null
+++ b/fluxcd/changelog.d/24510.added
@@ -0,0 +1 @@
+Add container-based config discovery support.
diff --git a/fluxcd/datadog_checks/fluxcd/config_models/discovery.py b/fluxcd/datadog_checks/fluxcd/config_models/discovery.py
new file mode 100644
index 0000000000000..75d49af525a70
--- /dev/null
+++ b/fluxcd/datadog_checks/fluxcd/config_models/discovery.py
@@ -0,0 +1,42 @@
+# (C) Datadog, Inc. 2026-present
+# All rights reserved
+# Licensed under a 3-clause BSD style license (see LICENSE)
+
+# This file is autogenerated.
+# To change this file you should edit assets/configuration/spec.yaml and then run the following commands:
+#     ddev -x validate config -s <INTEGRATION_NAME>
+#     ddev -x validate models -s <INTEGRATION_NAME>
+
+from __future__ import annotations
+
+from collections.abc import Iterator
+from typing import Any
+
+from datadog_checks.base.utils.discovery import Service, candidate_ports_by_name
+from datadog_checks.fluxcd.config_models import discovery_overrides
+from datadog_checks.fluxcd.config_models.instance import InstanceConfig
+from datadog_checks.fluxcd.config_models.shared import SharedConfig
+
+
+def _generated_candidates(service: Service) -> Iterator[dict[str, Any]]:
+    shared = SharedConfig.model_validate({}, context={'configured_fields': frozenset()}).model_dump(
+        by_alias=True, mode='json', exclude_none=True
+    )
+    # discovery[0]: from_named_ports
+    for port in candidate_ports_by_name(service, ['http-prom']):
+        ctx = {'port': port}
+        instance_data = {
+            'openmetrics_endpoint': 'http://{service.host}:{port.number}/metrics'.format(service=service, **ctx),
+        }
+        instance = InstanceConfig.model_validate(
+            instance_data, context={'configured_fields': frozenset(instance_data)}
+        ).model_dump(by_alias=True, mode='json', exclude_none=True)
+        yield {'init_config': shared, 'instances': [instance]}
+
+
+def candidates(service: Service) -> Iterator[dict[str, Any]]:
+    override = getattr(discovery_overrides, 'candidates', None)
+    if override is None:
+        yield from _generated_candidates(service)
+    else:
+        yield from override(service, default=_generated_candidates)
diff --git a/fluxcd/datadog_checks/fluxcd/config_models/discovery_overrides.py b/fluxcd/datadog_checks/fluxcd/config_models/discovery_overrides.py
new file mode 100644
index 0000000000000..66af68809dd4c
--- /dev/null
+++ b/fluxcd/datadog_checks/fluxcd/config_models/discovery_overrides.py
@@ -0,0 +1,12 @@
+# (C) Datadog, Inc. 2026-present
+# All rights reserved
+# Licensed under a 3-clause BSD style license (see LICENSE)
+
+# Override the generated discovery candidates() for this integration.
+#
+# Define a candidates(service, default) function to wrap or replace the generated
+# candidate generation. `default` is the generated generator; call it to reuse
+# the spec-driven candidates, or ignore it to replace them entirely.
+#
+# def candidates(service, default):
+#     yield from default(service)
diff --git a/fluxcd/datadog_checks/fluxcd/config_models/discovery_strategies.py b/fluxcd/datadog_checks/fluxcd/config_models/discovery_strategies.py
new file mode 100644
index 0000000000000..5ac036ddb4684
--- /dev/null
+++ b/fluxcd/datadog_checks/fluxcd/config_models/discovery_strategies.py
@@ -0,0 +1,18 @@
+# (C) Datadog, Inc. 2026-present
+# All rights reserved
+# Licensed under a 3-clause BSD style license (see LICENSE)
+
+# Here you can define custom (local:) discovery strategies for this integration.
+#
+# Decorate a generator with @discovery_strategy (imported from
+# datadog_checks.base.utils.discovery) and reference it from the spec discovery
+# stanza as `strategy: local:<function_name>`. The function receives the
+# discovered Service plus the inputs declared in the spec and yields one context
+# (ctx) mapping per candidate, exposing the keys listed in `provides`.
+#
+# from datadog_checks.base.utils.discovery import discovery_strategy
+#
+# @discovery_strategy(provides=('svc',))
+# def from_some_config(service, config_path):
+#     ...
+#     yield {'svc': ...}
diff --git a/fluxcd/datadog_checks/fluxcd/data/auto_conf.yaml b/fluxcd/datadog_checks/fluxcd/data/auto_conf.yaml
new file mode 100644
index 0000000000000..2eb738fcdb0be
--- /dev/null
+++ b/fluxcd/datadog_checks/fluxcd/data/auto_conf.yaml
@@ -0,0 +1,30 @@
+## @param ad_identifiers - list of strings - required
+## A list of container identifiers that are used by Autodiscovery to identify
+## which container the check should be run against. For more information, see:
+## https://docs.datadoghq.com/agent/guide/ad_identifiers/
+#
+ad_identifiers:
+  - helm-controller
+  - image-automation-controller
+  - image-reflector-controller
+  - kustomize-controller
+  - notification-controller
+  - source-controller
+
+## CEL selector for autodiscovery.
+#
+cel_selector:
+  containers:
+  - container.image.reference.contains("fluxcd/")
+
+## Enables configuration discovery
+#
+discovery: {}
+
+## Unused init configuration
+#
+init_config:
+
+## Unused instance configuration
+#
+instances: []
diff --git a/fluxcd/pyproject.toml b/fluxcd/pyproject.toml
index 180e6cbcaf1ef..6a09cb1c62609 100644
--- a/fluxcd/pyproject.toml
+++ b/fluxcd/pyproject.toml
@@ -28,7 +28,7 @@ classifiers = [
     "Private :: Do Not Upload",
 ]
 dependencies = [
-    "datadog-checks-base>=37.33.0",
+    "datadog-checks-base>=38.0.0",
 ]
 dynamic = [
     "version",
diff --git a/fluxcd/tests/conftest.py b/fluxcd/tests/conftest.py
index 7f921066e8155..bfe31ed4b3bd8 100644
--- a/fluxcd/tests/conftest.py
+++ b/fluxcd/tests/conftest.py
@@ -14,6 +14,7 @@
 from datadog_checks.fluxcd import FluxcdCheck
 
 HERE = get_here()
+CHECK_ROOT = os.path.dirname(HERE)
 opj = os.path.join
 
 # The Services in flux-system (source-controller, notification-controller) only expose the
@@ -25,6 +26,7 @@
 CONTROLLERS = ('source-controller', 'helm-controller', 'kustomize-controller', 'notification-controller')
 METRICS_PORT = 8080
 POD_IP_STATE_PREFIX = 'fluxcd_pod_ip_'
+KUBECONFIG_STATE = 'fluxcd_kubeconfig'
 
 
 def setup_fluxcd():
@@ -73,6 +75,7 @@ def get_controller_pod_ip(controller: str) -> str:
 @pytest.fixture(scope='session')
 def dd_environment():
     with kind_run(conditions=[setup_fluxcd]) as kubeconfig:
+        save_state(KUBECONFIG_STATE, kubeconfig)
         instances = [
             {
                 'openmetrics_endpoint': f'http://{get_state(POD_IP_STATE_PREFIX + controller)}:{METRICS_PORT}/metrics',
@@ -80,11 +83,22 @@ def dd_environment():
             for controller in CONTROLLERS
         ]
 
-        metadata = {'agent_type': 'kubernetes', 'kubernetes': {'kubeconfig': kubeconfig}}
+        metadata = {
+            'agent_type': 'kubernetes',
+            'kubernetes': {
+                'kubeconfig': kubeconfig,
+                'auto_conf': os.path.join(CHECK_ROOT, 'datadog_checks', 'fluxcd', 'data', 'auto_conf.yaml'),
+            },
+        }
 
         yield {'instances': instances}, metadata
 
 
+@pytest.fixture(scope='session')
+def fluxcd_kubeconfig():
+    return get_state(KUBECONFIG_STATE)
+
+
 @pytest.fixture
 def instance():
     return {
diff --git a/fluxcd/tests/test_e2e.py b/fluxcd/tests/test_e2e.py
index dc5742a58468e..c9931a981eb4b 100644
--- a/fluxcd/tests/test_e2e.py
+++ b/fluxcd/tests/test_e2e.py
@@ -2,18 +2,30 @@
 # All rights reserved
 # Licensed under a 3-clause BSD style license (see LICENSE)
 
+import pytest
+
+from datadog_checks.base.stubs.aggregator import AggregatorStub
+from datadog_checks.dev.kubernetes import assert_all_discovery_candidates_stable_kubernetes
 from datadog_checks.dev.utils import get_metadata_metrics
+from datadog_checks.fluxcd import FluxcdCheck
 
 from .common import EXPECTED_METRICS
 
+# All flux-system controllers deployed by the kind fixture and matched by the check's
+# ad_identifiers, including image-automation-controller, which the non-discovery E2E test's
+# fixed instance list omits. image-reflector-controller is also a valid ad_identifier but isn't
+# listed here: the kind fixture's install.yaml deliberately excludes its Deployment because it
+# never reached Ready in CI, so it has no running pod for the discovery E2E tests to exercise.
+ALL_CONTROLLERS = (
+    'source-controller',
+    'helm-controller',
+    'image-automation-controller',
+    'kustomize-controller',
+    'notification-controller',
+)
 
-def test_source_controller_metrics(dd_agent_check):
-    """
-    This only tests version 2 of flux.
 
-    Version 1 is in maintenance mode, all our users are on version 2.
-    """
-    aggregator = dd_agent_check()
+def assert_metrics(aggregator: AggregatorStub) -> None:
     ignore = {
         'fluxcd.controller.runtime.reconcile.count',
         'fluxcd.controller.runtime.reconcile.errors.count',
@@ -35,3 +47,33 @@ def test_source_controller_metrics(dd_agent_check):
         aggregator.assert_metric(metric_name)
     aggregator.assert_all_metrics_covered()
     aggregator.assert_metrics_using_metadata(get_metadata_metrics())
+
+
+def test_source_controller_metrics(dd_agent_check):
+    """
+    This only tests version 2 of flux.
+
+    Version 1 is in maintenance mode, all our users are on version 2.
+    """
+    aggregator = dd_agent_check()
+    assert_metrics(aggregator)
+
+
+@pytest.mark.e2e
+def test_e2e_discovery(dd_agent_check_discovery):
+    # Kubelet Autodiscovery is expected to find all five flux-system controller pods (the four
+    # exercised by the non-discovery E2E test above plus image-automation-controller).
+    aggregator = dd_agent_check_discovery(discovery_min_instances=len(ALL_CONTROLLERS))
+    assert_metrics(aggregator)
+
+
+@pytest.mark.e2e
+@pytest.mark.parametrize('controller', ALL_CONTROLLERS)
+def test_e2e_discovery_all_candidates(dd_agent_check, fluxcd_kubeconfig, controller):
+    assert_all_discovery_candidates_stable_kubernetes(
+        dd_agent_check,
+        FluxcdCheck,
+        fluxcd_kubeconfig,
+        namespace='flux-system',
+        pod_selector=f'app={controller}',
+    )