St Margaret's was founded in 1867 as a mission church by Father John Comper, one of the first followers in Scotland of the Oxford Movement.

[1][better source needed] Comper was at the time rector of St John's, Aberdeen's oldest Anglican congregation.

A separate church hall was built in 1908 by the architect George Irvine, and in the same year, Ninian Comper installed the aisle and oak screen.

The ichthus in the centre is a Greek anagram "Jesus Christ, God, Son, Saviour".

St Margaret's is one of few Scottish Episcopal congregations which has regular Gaelic Mass, having it on the first Saturday of the month at midday.