diff --git a/bundle/config/mutator/resourcemutator/apply_bundle_permissions.go b/bundle/config/mutator/resourcemutator/apply_bundle_permissions.go
index 15493ae9d15..da9fcc75c22 100644
--- a/bundle/config/mutator/resourcemutator/apply_bundle_permissions.go
+++ b/bundle/config/mutator/resourcemutator/apply_bundle_permissions.go
@@ -108,6 +108,12 @@ func (m *bundlePermissions) Apply(ctx context.Context, b *bundle.Bundle) diag.Di
 		return diag.FromErr(err)
 	}
 
+	// Target permissions follow root permissions when SelectTarget merges the lists.
+	targetPermissionsStart := len(b.Config.Permissions)
+	if b.Target != nil {
+		targetPermissionsStart -= len(b.Target.Permissions)
+	}
+
 	for _, group := range b.Config.Resources.AllResources() {
 		key := group.Description.PluralName
 		lm, ok := levelsMap[key]
@@ -124,6 +130,7 @@ func (m *bundlePermissions) Apply(ctx context.Context, b *bundle.Bundle) diag.Di
 				permissions,
 				key,
 				lm,
+				targetPermissionsStart,
 			)...)
 			writePermissions(field, permissions)
 		}
@@ -187,9 +194,10 @@ func convertPermissions(
 	resourcePermissions []resources.Permission,
 	resourceName string,
 	lm map[string]string,
+	targetPermissionsStart int,
 ) []resources.Permission {
 	var permissions []resources.Permission
-	for _, p := range bundlePermissions {
+	for i, p := range bundlePermissions {
 		level, ok := lm[string(p.Level)]
 		// If there is no bundle permission level defined in the map, it means
 		// it's not applicable for the resource, therefore skipping
@@ -197,7 +205,13 @@ func convertPermissions(
 			continue
 		}
 
-		if notifyForPermissionOverlap(ctx, p, resourcePermissions, resourceName) {
+		if i >= targetPermissionsStart && resourceName == "jobs" && p.GroupName != "" {
+			// A job-level group permission takes precedence over the target-level one.
+			overlap, _ := isPermissionOverlap(p, resourcePermissions, resourceName)
+			if overlap {
+				continue
+			}
+		} else if notifyForPermissionOverlap(ctx, p, resourcePermissions, resourceName) {
 			continue
 		}
 
diff --git a/bundle/config/mutator/resourcemutator/apply_bundle_permissions_test.go b/bundle/config/mutator/resourcemutator/apply_bundle_permissions_test.go
index 610832c2b92..037f06332f2 100644
--- a/bundle/config/mutator/resourcemutator/apply_bundle_permissions_test.go
+++ b/bundle/config/mutator/resourcemutator/apply_bundle_permissions_test.go
@@ -9,6 +9,7 @@ import (
 
 	"github.com/databricks/cli/bundle"
 	"github.com/databricks/cli/bundle/config"
+	"github.com/databricks/cli/bundle/config/mutator"
 	"github.com/databricks/cli/bundle/config/resources"
 	"github.com/databricks/cli/libs/diag"
 	"github.com/databricks/cli/libs/dyn"
@@ -223,6 +224,58 @@ func TestWarningOnOverlapPermission(t *testing.T) {
 	require.Contains(t, b.Config.Resources.Jobs["job_2"].Permissions, resources.JobPermission{Level: "CAN_VIEW", GroupName: "TestGroup"})
 }
 
+func TestTargetGroupPermissionOverridesJobWithoutWarning(t *testing.T) {
+	for _, tc := range []struct {
+		name            string
+		rootPermissions []resources.Permission
+		wantWarnings    int
+	}{
+		{name: "target only"},
+		{
+			name: "root and target",
+			rootPermissions: []resources.Permission{
+				{Level: permissions.CAN_VIEW, GroupName: "TestGroup"},
+			},
+			wantWarnings: 1,
+		},
+	} {
+		t.Run(tc.name, func(t *testing.T) {
+			b := &bundle.Bundle{
+				Config: config.Root{
+					Permissions: tc.rootPermissions,
+					Targets: map[string]*config.Target{
+						"dev-ci": {
+							Permissions: []resources.Permission{
+								{Level: permissions.CAN_VIEW, GroupName: "TestGroup"},
+							},
+							Resources: &config.Resources{
+								Jobs: map[string]*resources.Job{
+									"job_1": {
+										JobSettings: jobs.JobSettings{Name: "job_1"},
+										Permissions: []resources.JobPermission{
+											{Level: "CAN_MANAGE_RUN", GroupName: "TestGroup"},
+										},
+									},
+								},
+							},
+						},
+					},
+				},
+			}
+
+			diags := bundle.ApplySeq(t.Context(), b, mutator.SelectTarget("dev-ci"), ApplyBundlePermissions())
+			require.Len(t, diags, tc.wantWarnings)
+			if tc.wantWarnings > 0 {
+				require.Equal(t, diag.Warning, diags[0].Severity)
+				require.Equal(t, "'jobs' already has permissions set for 'TestGroup' group", diags[0].Summary)
+			}
+			require.Equal(t, []resources.JobPermission{
+				{Level: "CAN_MANAGE_RUN", GroupName: "TestGroup"},
+			}, b.Config.Resources.Jobs["job_1"].Permissions)
+		})
+	}
+}
+
 func TestAllResourcesExplicitlyDefinedForPermissionsSupport(t *testing.T) {
 	r := config.Resources{}