diff --git a/server/channels/api4/channel_test.go b/server/channels/api4/channel_test.go
index 1d4c1f515e..64140e2466 100644
--- a/server/channels/api4/channel_test.go
+++ b/server/channels/api4/channel_test.go
@@ -4801,6 +4801,29 @@ func TestMoveChannel(t *testing.T) {
 		require.Equal(t, team2.Id, ch.TeamId)
 	})
 
+	t.Run("Should return custom error with repeated channel", func(t *testing.T) {
+		channelT1 := &model.Channel{
+			DisplayName: "repeated",
+			Name:        "repeated",
+			Type:        model.ChannelTypePrivate,
+			TeamId:      team1.Id,
+		}
+		channelT1, _, err := th.Client.CreateChannel(context.TODO(), channelT1)
+		require.NoError(t, err)
+
+		channelT2 := &model.Channel{
+			DisplayName: "repeated",
+			Name:        "repeated",
+			Type:        model.ChannelTypePrivate,
+			TeamId:      team2.Id,
+		}
+		_, _, err = th.Client.CreateChannel(context.TODO(), channelT2)
+		require.NoError(t, err)
+
+		_, _, err = th.SystemAdminClient.MoveChannel(context.Background(), channelT1.Id, team2.Id, false)
+		require.EqualError(t, err, "A channel with that name already exists on the same team.")
+	})
+
 	t.Run("Should move private channel", func(t *testing.T) {
 		channel := th.CreatePrivateChannel()
 		ch, _, err := th.SystemAdminClient.MoveChannel(context.Background(), channel.Id, team1.Id, false)
diff --git a/server/channels/app/channel.go b/server/channels/app/channel.go
index f5f2d5331e..45986a12a5 100644
--- a/server/channels/app/channel.go
+++ b/server/channels/app/channel.go
@@ -622,12 +622,12 @@ func (a *App) UpdateChannel(c request.CTX, channel *model.Channel) (*model.Chann
 	_, err := a.Srv().Store().Channel().Update(c, channel)
 	if err != nil {
 		var appErr *model.AppError
+		var uniqueConstraintErr *store.ErrUniqueConstraint
 		var invErr *store.ErrInvalidInput
 		switch {
+		case errors.As(err, &uniqueConstraintErr):
+			return nil, model.NewAppError("UpdateChannel", store.ChannelExistsError, nil, "", http.StatusBadRequest).Wrap(err)
 		case errors.As(err, &invErr):
-			if invErr.Entity == "Channel" && invErr.Field == "Name" {
-				return nil, model.NewAppError("UpdateChannel", store.ChannelExistsError, nil, "", http.StatusBadRequest).Wrap(err)
-			}
 			return nil, model.NewAppError("UpdateChannel", "app.channel.update.bad_id", nil, "", http.StatusBadRequest).Wrap(err)
 		case errors.As(err, &appErr):
 			return nil, appErr
@@ -3149,10 +3149,13 @@ func (a *App) MoveChannel(c request.CTX, team *model.Team, channel *model.Channe
 	channel.TeamId = team.Id
 	if _, err := a.Srv().Store().Channel().Update(c, channel); err != nil {
 		var appErr *model.AppError
+		var uniqueConstraintErr *store.ErrUniqueConstraint
 		var invErr *store.ErrInvalidInput
 		switch {
 		case errors.As(err, &invErr):
 			return model.NewAppError("MoveChannel", "app.channel.update.bad_id", nil, "", http.StatusBadRequest).Wrap(err)
+		case errors.As(err, &uniqueConstraintErr):
+			return model.NewAppError("MoveChannel", store.ChannelExistsError, nil, "", http.StatusBadRequest).Wrap(err)
 		case errors.As(err, &appErr):
 			return appErr
 		default:
diff --git a/server/channels/store/sqlstore/channel_store.go b/server/channels/store/sqlstore/channel_store.go
index a845a1ca43..b0957f39cf 100644
--- a/server/channels/store/sqlstore/channel_store.go
+++ b/server/channels/store/sqlstore/channel_store.go
@@ -745,7 +745,7 @@ func (s SqlChannelStore) updateChannelT(transaction *sqlxTxWrapper, channel *mod
 		WHERE Id=:Id`, channel)
 	if err != nil {
 		if IsUniqueConstraintError(err, []string{"Name", "channels_name_teamid_key"}) {
-			return nil, store.NewErrInvalidInput("Channel", "Name", channel.Name)
+			return nil, store.NewErrUniqueConstraint("Name")
 		}
 		return nil, errors.Wrapf(err, "failed to update channel with id=%s", channel.Id)
 	}
diff --git a/server/channels/store/storetest/channel_store.go b/server/channels/store/storetest/channel_store.go
index 4bb0a75f60..60a2cbc2c3 100644
--- a/server/channels/store/storetest/channel_store.go
+++ b/server/channels/store/storetest/channel_store.go
@@ -364,10 +364,9 @@ func testChannelStoreUpdate(t *testing.T, rctx request.CTX, ss store.Store) {
 
 	// Make sure that the error correctly reports the wrong field to be Name
 	// See https://mattermost.atlassian.net/browse/MM-53756
-	var invalidInputErr *store.ErrInvalidInput
-	require.ErrorAs(t, err, &invalidInputErr)
-	require.Equal(t, invalidInputErr.Entity, "Channel")
-	require.Equal(t, invalidInputErr.Field, "Name")
+	var uniqueConstraintErr *store.ErrUniqueConstraint
+	require.ErrorAs(t, err, &uniqueConstraintErr)
+	require.Contains(t, uniqueConstraintErr.Columns, "Name")
 }
 
 func testGetChannelUnread(t *testing.T, rctx request.CTX, ss store.Store) {