Huddlestone, who has succeeded Paul McShane in the role, turned professional at Derby County in 2002, and he has also represented Tottenham Hotspur, Wolverhampton Wanderers and Hull City during a long career.
The 35-year-old - a four-time England international - left Hull at the end of June following the expiration of his contract, but he has now made the switch to Old Trafford as a player-coach.
The Englishman has moved to the club alongside David Hughes, who will be a professional development phase coach for the 20-time English champions.
"The experienced midfielder will create various unique development opportunities for United's Academy players by coaching from within training sessions and driving daily standards on and off the pitch," read a statement on Man United's official website.
Head of Academy Nick Cox told the club's official website: "We are really pleased to add both Tom and David to our team of best-in-class coaching experts working across the Professional Development Phase.
"The innovative approach that we took in appointing a playing coach last season was a real success and brought a range of benefits to the whole Academy.
"Tom is a superb candidate to take on this important role. Having played at the highest level during his outstanding career and already displayed excellent capabilities as a coach, his presence will benefit our players immeasurably.
"David brings a fantastic wealth of coaching and leadership experience. He has a proven track record of developing a great number of players who are playing in the Premier League and throughout professional football.
"David and Tom join a world-class team of coaches, led by Travis Binnion, who will continue to develop players for our first team and build on the legacy of our world-leading youth development system."
Man United have also confirmed that Huddlestone will be available to play for the team's Under-21s in Premier League 2 and the EFL Trophy, providing that he comes through a medical.
Hughes, meanwhile, has recently been academy manager at Cardiff City, while he has had roles at Southampton and Aston Villa during his coaching career.
Matt Walker and Curtis Quinn have also arrived, with the duo due to work as head of PDP athletic development and in the analysis department respectively.
Man United are currently preparing for their 2022-23 Premier League opener against Brighton & Hove Albion, which takes place at Old Trafford on Sunday afternoon.