diff --git a/pkg/spec/gitops.go b/pkg/spec/gitops.go
index d4c5a889762..afb2dca4021 100644
--- a/pkg/spec/gitops.go
+++ b/pkg/spec/gitops.go
@@ -1,6 +1,7 @@
 package spec
 
 import (
+	"bytes"
 	"encoding/json"
 	"errors"
 	"fmt"
@@ -16,6 +17,8 @@ import (
 	"github.com/bmatcuk/doublestar/v4"
 	"github.com/fleetdm/fleet/v4/pkg/optjson"
 	"github.com/fleetdm/fleet/v4/server/fleet"
+	apple_mdm "github.com/fleetdm/fleet/v4/server/mdm/apple"
+	"github.com/fleetdm/fleet/v4/server/mdm/microsoft/syncml"
 	"github.com/fleetdm/fleet/v4/server/ptr"
 	"github.com/ghodss/yaml"
 	"github.com/hashicorp/go-multierror"
@@ -1206,9 +1209,86 @@ func parseControls(top map[string]json.RawMessage, result *GitOps, logFn Logf, y
 		result.Controls.AndroidSettings = androidSettings
 	}
 
+	if err := validateOSUpdatesProfileConflict(result.Controls); err != nil {
+		multiError = multierror.Append(multiError, err)
+	}
+
 	return multiError
 }
 
+// validateOSUpdatesProfileConflict rejects a config that both configures managed
+// OS updates and includes a custom configuration profile that enforces OS
+// updates. The server checks it for non-dry runs; we replicate it here against
+// the incoming payload so dry-runs fail too.
+func validateOSUpdatesProfileConflict(controls GitOpsControls) error {
+	macOSConfigured := osUpdatesConfigured[fleet.AppleOSUpdateSettings](controls.MacOSUpdates)
+	iOSConfigured := osUpdatesConfigured[fleet.AppleOSUpdateSettings](controls.IOSUpdates)
+	iPadOSConfigured := osUpdatesConfigured[fleet.AppleOSUpdateSettings](controls.IPadOSUpdates)
+	if macOSConfigured || iOSConfigured || iPadOSConfigured {
+		macOSSettings, _ := controls.MacOSSettings.(fleet.MacOSSettings)
+		for _, profile := range macOSSettings.CustomSettings {
+			contains, err := profileFileContains(profile.Path, apple_mdm.DeclarationTypeSoftwareUpdate)
+			if err != nil {
+				return err
+			}
+			if contains {
+				return fmt.Errorf("controls.apple_settings.configuration_profiles[]: %s", fleet.OSUpdatesAlreadyConfiguredErrorMessage)
+			}
+		}
+	}
+
+	windowsConfigured := osUpdatesConfigured[fleet.WindowsUpdates](controls.WindowsUpdates)
+	if windowsConfigured {
+		windowsSettings, _ := controls.WindowsSettings.(fleet.WindowsSettings)
+		for _, profile := range windowsSettings.CustomSettings.Value {
+			contains, err := profileFileContains(profile.Path, syncml.FleetOSUpdateTargetLocURI)
+			if err != nil {
+				return err
+			}
+			if contains {
+				return fmt.Errorf("controls.windows_settings.configuration_profiles[]: %s", fleet.OSUpdatesAlreadyConfiguredErrorMessage)
+			}
+		}
+	}
+
+	return nil
+}
+
+// osUpdatesSettings is implemented by the OS update settings types that report
+// whether managed OS updates are configured.
+type osUpdatesSettings interface {
+	Configured() bool
+}
+
+// osUpdatesConfigured unmarshals the raw controls value (e.g. controls.macos_updates)
+// into T and reports whether it configures managed OS updates.
+func osUpdatesConfigured[T osUpdatesSettings](v any) bool {
+	if v == nil {
+		return false
+	}
+	data, err := json.Marshal(v)
+	if err != nil {
+		return false
+	}
+	var settings T
+	if err := json.Unmarshal(data, &settings); err != nil {
+		return false
+	}
+	return settings.Configured()
+}
+
+// profileFileContains reports whether the profile file at path contains needle.
+func profileFileContains(path, needle string) (bool, error) {
+	if path == "" {
+		return false, nil
+	}
+	fileBytes, err := os.ReadFile(path)
+	if err != nil {
+		return false, fmt.Errorf("failed to read profile file %s: %v", path, err)
+	}
+	return bytes.Contains(fileBytes, []byte(needle)), nil
+}
+
 func processControlsPathIfNeeded(controlsTop GitOpsControls, result *GitOps, controlsFilePath *string) []error {
 	if controlsTop.Path == nil {
 		result.Controls = controlsTop
diff --git a/pkg/spec/gitops_test.go b/pkg/spec/gitops_test.go
index 75d7df70911..13f1dffa094 100644
--- a/pkg/spec/gitops_test.go
+++ b/pkg/spec/gitops_test.go
@@ -2952,6 +2952,96 @@ func TestGitOpsGlobProfiles(t *testing.T) {
 	})
 }
 
+func TestGitOpsOSUpdatesProfileConflict(t *testing.T) {
+	t.Parallel()
+
+	const appleDecl = `{"Type":"com.apple.configuration.softwareupdate.enforcement.specific","Identifier":"x","Payload":{}}`
+	const windowsProfile = `<Replace><Item><Target><LocURI>./Vendor/MSFT/Policy/Config/Update/x</LocURI></Target></Item></Replace>`
+
+	t.Run("macos updates configured with software update declaration fails", func(t *testing.T) {
+		t.Parallel()
+		dir := t.TempDir()
+		require.NoError(t, os.WriteFile(filepath.Join(dir, "su.json"), []byte(appleDecl), 0o644))
+
+		config := getGlobalConfig([]string{"controls"})
+		config += `controls:
+  macos_updates:
+    minimum_version: "14.0"
+    deadline: "2024-01-01"
+  apple_settings:
+    configuration_profiles:
+      - path: su.json
+`
+		yamlPath := filepath.Join(dir, "gitops.yml")
+		require.NoError(t, os.WriteFile(yamlPath, []byte(config), 0o644))
+
+		_, err := GitOpsFromFile(yamlPath, dir, nil, nopLogf)
+		require.Error(t, err)
+		assert.Contains(t, err.Error(), fleet.OSUpdatesAlreadyConfiguredErrorMessage)
+	})
+
+	t.Run("windows updates configured with software update profile fails", func(t *testing.T) {
+		t.Parallel()
+		dir := t.TempDir()
+		require.NoError(t, os.WriteFile(filepath.Join(dir, "su.xml"), []byte(windowsProfile), 0o644))
+
+		config := getGlobalConfig([]string{"controls"})
+		config += `controls:
+  windows_updates:
+    deadline_days: 5
+    grace_period_days: 1
+  windows_settings:
+    configuration_profiles:
+      - path: su.xml
+`
+		yamlPath := filepath.Join(dir, "gitops.yml")
+		require.NoError(t, os.WriteFile(yamlPath, []byte(config), 0o644))
+
+		_, err := GitOpsFromFile(yamlPath, dir, nil, nopLogf)
+		require.Error(t, err)
+		assert.Contains(t, err.Error(), fleet.OSUpdatesAlreadyConfiguredErrorMessage)
+	})
+
+	t.Run("software update declaration without configured os updates is allowed", func(t *testing.T) {
+		t.Parallel()
+		dir := t.TempDir()
+		require.NoError(t, os.WriteFile(filepath.Join(dir, "su.json"), []byte(appleDecl), 0o644))
+
+		config := getGlobalConfig([]string{"controls"})
+		config += `controls:
+  apple_settings:
+    configuration_profiles:
+      - path: su.json
+`
+		yamlPath := filepath.Join(dir, "gitops.yml")
+		require.NoError(t, os.WriteFile(yamlPath, []byte(config), 0o644))
+
+		_, err := GitOpsFromFile(yamlPath, dir, nil, nopLogf)
+		require.NoError(t, err)
+	})
+
+	t.Run("macos updates configured with non-conflicting profile is allowed", func(t *testing.T) {
+		t.Parallel()
+		dir := t.TempDir()
+		require.NoError(t, os.WriteFile(filepath.Join(dir, "plain.mobileconfig"), []byte("<plist></plist>"), 0o644))
+
+		config := getGlobalConfig([]string{"controls"})
+		config += `controls:
+  macos_updates:
+    minimum_version: "14.0"
+    deadline: "2024-01-01"
+  apple_settings:
+    configuration_profiles:
+      - path: plain.mobileconfig
+`
+		yamlPath := filepath.Join(dir, "gitops.yml")
+		require.NoError(t, os.WriteFile(yamlPath, []byte(config), 0o644))
+
+		_, err := GitOpsFromFile(yamlPath, dir, nil, nopLogf)
+		require.NoError(t, err)
+	})
+}
+
 func TestUnknownKeyDetection(t *testing.T) {
 	t.Parallel()