The church dates back to 1190, when it was founded by David, Earl of Huntingdon, brother of William the Lion, King of Scots.

In the late Middle Ages, Dundee's was the largest parish church in Scotland with the Old Steeple, built in the 1470s during the Provostship of George Spalding, the tallest tower.

Several past ministers have served as Moderators of the General Assembly of the Church of Scotland, most recently the late Very Reverend Dr William B. R. Macmillan in 1991.

The incumbent minister of the Parish of Dundee, Henry Scrymgeour demitted office in 1690 and the charge was declared vacant in 1694.

[4] A new memorial and roll of honour to commemorate over 600 local seamen and women who died during the Great War was placed in the church in 2017.