The 20-year-old midfielder, who has signed a three-year deal, is the Dons' fourth signing of the summer and comes just a day after boss Roberto Di Matteo left the club to take over at West Brom.
Gleeson, who spent time on loan at stadium:mk last season, told the club's official website: "I'd planned to come back here if I got the chance and it's great that the two clubs have got the deal finalised.
"Obviously the chairman is looking for a new manager, but the club itself has huge ambition and that's good enough for me. As a player I have ambitions myself and I feel I can achieve those here."
Dons chairman Pete Winkelman added: "It's a fantastic signing for the club - Stephen made a huge impression here last season and is just they type of young player that can help take us forward."