diff --git a/pkg/services/ngalert/models/alert_rule_test.go b/pkg/services/ngalert/models/alert_rule_test.go
index 22d2f65a9e6..f875a73d9d7 100644
--- a/pkg/services/ngalert/models/alert_rule_test.go
+++ b/pkg/services/ngalert/models/alert_rule_test.go
@@ -347,7 +347,7 @@ func TestPatchPartialAlertRule(t *testing.T) {
 			t.Run(testCase.name, func(t *testing.T) {
 				var existing *AlertRule
 				for {
-					existing = AlertRuleGen()()
+					existing = AlertRuleGen(WithUniqueID())()
 					cloned := *existing
 					// make sure the generated rule does not match the mutated one
 					testCase.mutator(&cloned)
diff --git a/pkg/services/ngalert/models/testing.go b/pkg/services/ngalert/models/testing.go
index 71ffd9312a9..f22f357f251 100644
--- a/pkg/services/ngalert/models/testing.go
+++ b/pkg/services/ngalert/models/testing.go
@@ -71,7 +71,7 @@ func AlertRuleGen(mutators ...AlertRuleMutator) func() *AlertRule {
 		}
 
 		rule := &AlertRule{
-			ID:                   rand.Int63n(1500),
+			ID:                   0,
 			OrgID:                rand.Int63n(1500) + 1, // Prevent OrgID=0 as this does not pass alert rule validation.
 			Title:                "TEST-ALERT-" + util.GenerateShortUID(),
 			Condition:            "A",
@@ -110,7 +110,7 @@ func WithUniqueID() AlertRuleMutator {
 	usedID := make(map[int64]struct{})
 	return func(rule *AlertRule) {
 		for {
-			id := rand.Int63n(1500)
+			id := rand.Int63n(1500) + 1
 			if _, ok := usedID[id]; !ok {
 				usedID[id] = struct{}{}
 				rule.ID = id
diff --git a/pkg/services/ngalert/store/alert_rule.go b/pkg/services/ngalert/store/alert_rule.go
index 2570657ea01..0ae77f063d5 100644
--- a/pkg/services/ngalert/store/alert_rule.go
+++ b/pkg/services/ngalert/store/alert_rule.go
@@ -169,7 +169,7 @@ 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.ErrAlertRuleConflict(newRules[i], ngmodels.ErrAlertRuleUniqueConstraintViolation)
+						return ruleConstraintViolationToErr(newRules[i], err)
 					}
 					return fmt.Errorf("failed to create new rules: %w", err)
 				}
@@ -215,7 +215,7 @@ 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.ErrAlertRuleConflict(r.New, ngmodels.ErrAlertRuleUniqueConstraintViolation)
+						return ruleConstraintViolationToErr(r.New, err)
 					}
 					return fmt.Errorf("failed to update rule [%s] %s: %w", r.New.UID, r.New.Title, err)
 				}
@@ -758,3 +758,14 @@ func (st DBstore) RenameReceiverInNotificationSettings(ctx context.Context, orgI
 	}
 	return len(updates), st.UpdateAlertRules(ctx, updates)
 }
+
+func ruleConstraintViolationToErr(rule ngmodels.AlertRule, err error) error {
+	msg := err.Error()
+	if strings.Contains(msg, "UQE_alert_rule_org_id_namespace_uid_title") || strings.Contains(msg, "alert_rule.org_id, alert_rule.namespace_uid, alert_rule.title") {
+		return ngmodels.ErrAlertRuleConflict(rule, ngmodels.ErrAlertRuleUniqueConstraintViolation)
+	} else if strings.Contains(msg, "UQE_alert_rule_org_id_uid") || strings.Contains(msg, "alert_rule.org_id, alert_rule.uid") {
+		return ngmodels.ErrAlertRuleConflict(rule, errors.New("rule UID under the same organisation should be unique"))
+	} else {
+		return ngmodels.ErrAlertRuleConflict(rule, err)
+	}
+}
diff --git a/pkg/services/ngalert/store/alert_rule_test.go b/pkg/services/ngalert/store/alert_rule_test.go
index 97aa3433d3e..fe470991d73 100644
--- a/pkg/services/ngalert/store/alert_rule_test.go
+++ b/pkg/services/ngalert/store/alert_rule_test.go
@@ -603,6 +603,7 @@ func TestIntegrationInsertAlertRules(t *testing.T) {
 		t.Skip("skipping integration test")
 	}
 
+	orgID := int64(1)
 	sqlStore := db.InitTestDB(t)
 	cfg := setting.NewCfg()
 	cfg.UnifiedAlerting.BaseInterval = 1 * time.Second
@@ -613,7 +614,7 @@ func TestIntegrationInsertAlertRules(t *testing.T) {
 		Cfg:           cfg.UnifiedAlerting,
 	}
 
-	rules := models.GenerateAlertRules(5, models.AlertRuleGen(models.WithOrgID(1), withIntervalMatching(store.Cfg.BaseInterval)))
+	rules := models.GenerateAlertRules(5, models.AlertRuleGen(models.WithOrgID(orgID), withIntervalMatching(store.Cfg.BaseInterval)))
 	deref := make([]models.AlertRule, 0, len(rules))
 	for _, rule := range rules {
 		deref = append(deref, *rule)
@@ -641,14 +642,30 @@ 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)
+	t.Run("fail to insert rules with same ID", func(t *testing.T) {
+		_, err = store.InsertAlertRules(context.Background(), []models.AlertRule{deref[0]})
+		require.ErrorIs(t, err, models.ErrAlertRuleConflictBase)
+	})
+	t.Run("fail insert rules with the same title in a folder", func(t *testing.T) {
+		cp := models.CopyRule(&deref[0])
+		cp.UID = cp.UID + "-new"
+		_, err = store.InsertAlertRules(context.Background(), []models.AlertRule{*cp})
+		require.ErrorIs(t, err, models.ErrAlertRuleConflictBase)
+		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)
+	})
+	t.Run("should not let insert rules with the same UID", func(t *testing.T) {
+		cp := models.CopyRule(&deref[0])
+		cp.Title = "unique-test-title"
+		_, err = store.InsertAlertRules(context.Background(), []models.AlertRule{*cp})
+		require.ErrorIs(t, err, models.ErrAlertRuleConflictBase)
+		require.ErrorContains(t, err, "rule UID under the same organisation should be unique")
+	})
 }
 
 func TestIntegrationAlertRulesNotificationSettings(t *testing.T) {