He first became a shareholder with his wife Pam in May 2011 as the Tayside outfit came out of administration.
Colvin was then named chairman in 2013 when the Football Partners Scotland consortium took control. FPS have now acquired his shareholding.
Tim Keyes will join the board as a replacement subject to passing the SFA’s fit and proper person requirements.
His appointment as a director is expected to be confirmed at the club’s next board meeting next month.
Colvin said: “The football club is in a much better financial position and a more stable managerial position than it was when Pam first got me involved back in late 2010, early 2011.
“This season’s top-six SPFL finish is where this club should be and I was delighted to see all the hard work done by John Nelms, Paul Hartley and the rest of the team at Dens Park paying off for the fantastic Dee fans.
“I know I leave the club in the very safe hands of John and particularly the Keyes family, who will be superb custodians of this famous football club.”