Dundee-born Holt played his part in all of Dundee United's successes in the 1980s, breaking into the first team in 1974 along with the likes of David Narey and Andy Gray, and made regular appearances in midfield or defence for the club until 1987, when he left for Dunfermline. A playing spell at Dundee followed, before player/manager spells with Forfar Athletic, Deveronvale and Montrose. Holt returned to United and Tannadice in the mid-1990s and spent several years in many coaching roles, before leaving in 2003 when Ian McCall was appointed Dundee United manager. He went on to become a scout for Celtic, operating in the Dundee area, before joining Dundee as youth development coach. Referred to by some fans as "Yosser" Holt, after hard man Yosser Hughes from the BBC's "Boys from the Black Stuff" mini series (1982), opponents feared Holt as he prowled around in midfield or gave opposition wingers a torrid time as a full back. But he was also a player blessed with tremendous ability; he was the man of the match at the Nou Camp in the UEFA Cup quarter final in 1987, shortly before his departure from Tannadice, as Dundee United beat Barcelona 2-1 on the night and 3-1 on aggregate to attain a 100% competitive record against the Catalan giants.
On May 10, 2012, John Holt moved on to take an academy role at Dundee United.