Maguire, who attended St Mary's Roman Catholic High School in Chesterfield, fell victim to the boo-boys when his name was announced on the team line-ups ahead of the 3-0 win on Tuesday night.
"I thought the reception was a joke. An absolute joke," Southgate told Sky Sports. "What he's done for us and the way he has performed for England has been phenomenal. I don't get it.
"We're either all in this together or we're not. He's in an England shirt and not only should you support someone in an England shirt regardless but when he's played at the level he has, it should be total commitment behind him. So, I don't get it.
"He was pretty faultless, stepping out from the back for the first goal and was involved in the second goal. This team is totally united. We recognise people have difficult moments but he's top player and will come through it."
Maguire has endured a difficult spell with Manchester United this season and has increasingly become the subject for ridicule on social media.