diff --git a/pkg/services/ngalert/models/alert_rule.go b/pkg/services/ngalert/models/alert_rule.go
index b10bdfab314..881fc311d87 100644
--- a/pkg/services/ngalert/models/alert_rule.go
+++ b/pkg/services/ngalert/models/alert_rule.go
@@ -27,7 +27,7 @@ var (
 	ErrCannotEditNamespace                = errors.New("user does not have permissions to edit the namespace")
 	ErrRuleGroupNamespaceNotFound         = errors.New("rule group not found under this namespace")
 	ErrAlertRuleFailedValidation          = errors.New("invalid alert rule")
-	ErrAlertRuleUniqueConstraintViolation = errors.New("a conflicting alert rule is found: rule title under the same organisation and folder should be unique")
+	ErrAlertRuleUniqueConstraintViolation = errors.New("rule title under the same organisation and folder should be unique")
 	ErrQuotaReached                       = errors.New("quota has been exceeded")
 	// ErrNoDashboard is returned when the alert rule does not have a Dashboard UID
 	// in its annotations or the dashboard does not exist.
diff --git a/pkg/services/ngalert/models/errors.go b/pkg/services/ngalert/models/errors.go
new file mode 100644
index 00000000000..9851d1c5919
--- /dev/null
+++ b/pkg/services/ngalert/models/errors.go
@@ -0,0 +1,15 @@
+package models
+
+import (
+	"github.com/grafana/grafana/pkg/util/errutil"
+)
+
+var (
+	errAlertRuleConflictMsg  = "conflicting alert rule found [rule_uid: '{{ .Public.RuleUID }}', title: '{{ .Public.Title }}', namespace_uid: '{{ .Public.NamespaceUID }}']: {{ .Public.Error }}"
+	ErrAlertRuleConflictBase = errutil.Conflict("alerting.alert-rule.conflict").
+					MustTemplate(errAlertRuleConflictMsg, errutil.WithPublic(errAlertRuleConflictMsg))
+)
+
+func ErrAlertRuleConflict(rule AlertRule, underlying error) error {
+	return ErrAlertRuleConflictBase.Build(errutil.TemplateData{Public: map[string]any{"RuleUID": rule.UID, "Title": rule.Title, "NamespaceUID": rule.NamespaceUID, "Error": underlying.Error()}, Error: underlying})
+}
diff --git a/pkg/services/ngalert/store/alert_rule.go b/pkg/services/ngalert/store/alert_rule.go
index 19c75ea82d4..585ddf14261 100644
--- a/pkg/services/ngalert/store/alert_rule.go
+++ b/pkg/services/ngalert/store/alert_rule.go
@@ -165,7 +165,7 @@ func (st DBstore) InsertAlertRules(ctx context.Context, rules []ngmodels.AlertRu
 			for i := range newRules {
 				if _, err := sess.Insert(&newRules[i]); err != nil {
 					if st.SQLStore.GetDialect().IsUniqueConstraintViolation(err) {
-						return ngmodels.ErrAlertRuleUniqueConstraintViolation
+						return ngmodels.ErrAlertRuleConflict(newRules[i], ngmodels.ErrAlertRuleUniqueConstraintViolation)
 					}
 					return fmt.Errorf("failed to create new rules: %w", err)
 				}
@@ -208,7 +208,7 @@ func (st DBstore) UpdateAlertRules(ctx context.Context, rules []ngmodels.UpdateR
 			if updated, err := sess.ID(r.Existing.ID).AllCols().Update(r.New); err != nil || updated == 0 {
 				if err != nil {
 					if st.SQLStore.GetDialect().IsUniqueConstraintViolation(err) {
-						return ngmodels.ErrAlertRuleUniqueConstraintViolation
+						return ngmodels.ErrAlertRuleConflict(r.New, ngmodels.ErrAlertRuleUniqueConstraintViolation)
 					}
 					return fmt.Errorf("failed to update rule [%s] %s: %w", r.New.UID, r.New.Title, err)
 				}
diff --git a/pkg/services/ngalert/store/alert_rule_test.go b/pkg/services/ngalert/store/alert_rule_test.go
index 1313ea028b4..844173297d6 100644
--- a/pkg/services/ngalert/store/alert_rule_test.go
+++ b/pkg/services/ngalert/store/alert_rule_test.go
@@ -317,6 +317,28 @@ func TestIntegrationUpdateAlertRulesWithUniqueConstraintViolation(t *testing.T)
 		require.Equal(t, newRule3.Title, dbrule3.Title)
 		require.Equal(t, newRule4.Title, dbrule4.Title)
 	})
+
+	t.Run("should fail with unique constraint violation", func(t *testing.T) {
+		rule1 := createRuleInFolder("unique-rule1", 1, "my-namespace")
+		rule2 := createRuleInFolder("unique-rule2", 1, "my-namespace")
+
+		newRule1 := models.CopyRule(rule1)
+		newRule2 := models.CopyRule(rule2)
+		newRule2.Title = newRule1.Title
+
+		err := store.UpdateAlertRules(context.Background(), []models.UpdateRule{{
+			Existing: rule2,
+			New:      *newRule2,
+		},
+		})
+		require.ErrorIs(t, err, models.ErrAlertRuleUniqueConstraintViolation)
+		require.NotEqual(t, newRule2.UID, "")
+		require.NotEqual(t, newRule2.Title, "")
+		require.NotEqual(t, newRule2.NamespaceUID, "")
+		require.ErrorContains(t, err, newRule2.UID)
+		require.ErrorContains(t, err, newRule2.Title)
+		require.ErrorContains(t, err, newRule2.NamespaceUID)
+	})
 }
 
 func TestIntegration_GetAlertRulesForScheduling(t *testing.T) {
@@ -617,6 +639,15 @@ func TestIntegrationInsertAlertRules(t *testing.T) {
 		}
 		require.Truef(t, found, "Rule with key %#v was not found in database", keyWithID)
 	}
+
+	_, err = store.InsertAlertRules(context.Background(), []models.AlertRule{deref[0]})
+	require.ErrorIs(t, err, models.ErrAlertRuleUniqueConstraintViolation)
+	require.NotEqual(t, deref[0].UID, "")
+	require.NotEqual(t, deref[0].Title, "")
+	require.NotEqual(t, deref[0].NamespaceUID, "")
+	require.ErrorContains(t, err, deref[0].UID)
+	require.ErrorContains(t, err, deref[0].Title)
+	require.ErrorContains(t, err, deref[0].NamespaceUID)
 }
 
 // createAlertRule creates an alert rule in the database and returns it.
diff --git a/pkg/tests/api/alerting/api_ruler_test.go b/pkg/tests/api/alerting/api_ruler_test.go
index 5844a387c22..e634492f224 100644
--- a/pkg/tests/api/alerting/api_ruler_test.go
+++ b/pkg/tests/api/alerting/api_ruler_test.go
@@ -841,11 +841,11 @@ func TestIntegrationAlertRuleConflictingTitle(t *testing.T) {
 		rulesWithUID.Rules = append(rulesWithUID.Rules, rules.Rules[0]) // Create new copy of first rule.
 
 		_, status, body := apiClient.PostRulesGroupWithStatus(t, "folder1", &rulesWithUID)
-		assert.Equal(t, http.StatusInternalServerError, status)
+		assert.Equal(t, http.StatusConflict, status)
 
 		var res map[string]any
 		require.NoError(t, json.Unmarshal([]byte(body), &res))
-		require.Equal(t, "failed to update rule group: failed to add rules: a conflicting alert rule is found: rule title under the same organisation and folder should be unique", res["message"])
+		require.Contains(t, res["message"], ngmodels.ErrAlertRuleUniqueConstraintViolation.Error())
 	})
 
 	t.Run("trying to update an alert to the title of an existing alert in the same folder should fail", func(t *testing.T) {
@@ -853,11 +853,11 @@ func TestIntegrationAlertRuleConflictingTitle(t *testing.T) {
 		rulesWithUID.Rules[1].GrafanaManagedAlert.Title = "AlwaysFiring"
 
 		_, status, body := apiClient.PostRulesGroupWithStatus(t, "folder1", &rulesWithUID)
-		assert.Equal(t, http.StatusInternalServerError, status)
+		assert.Equal(t, http.StatusConflict, status)
 
 		var res map[string]any
 		require.NoError(t, json.Unmarshal([]byte(body), &res))
-		require.Equal(t, "failed to update rule group: failed to update rules: a conflicting alert rule is found: rule title under the same organisation and folder should be unique", res["message"])
+		require.Contains(t, res["message"], ngmodels.ErrAlertRuleUniqueConstraintViolation.Error())
 	})
 
 	t.Run("trying to create alert with same title under another folder should succeed", func(t *testing.T) {