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Dempster was promoted to the position of Mansfield Town manager when Flitcroft's contract was terminated 14 May 2019.

Dempster accepted the position of academy manager at Mansfield at the end of the 2014–15 season. On the resignation of club manager Steve Evans in February 2018, Dempster assumed the role of caretaker manager, until new manager David Flitcroft was confirmed 1 March 2018.

In May 2012, Dempster was released by Crawley after being deemed surplus to requirements following a handful of League 2 appearances that year and a loan spell at Conference Premier club Mansfield Town. He signed for Mansfield permanently for the 2012/13 season. After an injury and a spell on loan at Tamworth, Dempster established himself as a regular in the side that went on to win the Conference Premier on the last day of the season. Dempster signed a new contract at The Stags for 2013/14, making a return to the Football League. He captained the team in the absence of Adam Murray.

Following a string of impressive performances for Kettering Town, Dempster was signed by Crawley Town for an undisclosed fee in the 2011 transfer window, in the middle of their promotion-winning season that saw Crawley elevated to the Football League.

From 2007 he has been playing for Kettering Town, where he captained the side to promotion to the Conference Premier, and was awarded Players' Player and Supporters' player.

In 2006 Dempster signed for Oxford United during the January transfer window.

He was also selected for Paul Fairclough's England National XI side back in 2006.

John Dempster (born 1 April 1983) is a professional football manager and former player who played as a centre back. He was most recently the manager of League Two club Mansfield Town.