The 49-year-old has signed a two-and-a-half-year deal with the Scottish Premiership club.
Inverness had been in search of a boss following Terry Butcher's departure to Hibernian on November 12.
"He is an experienced manager which is what we feel is required in the current scenario we have at our club," chairman Kenny Cameron told the team's official website.
"He greatly impressed all the directors with his knowledge of the club, his passion and philosophy for the game.
"John has been chosen from a high-calibre short list who were a pleasure to interview. He has the drive and coaching expertise to be an excellent asset to Caley Thistle and run the football department in a highly motivated and professional manner."
Inverness, who are currently in second place in the Scottish Premiership table, travel to St Mirren in the league on Saturday.