The church was first referred to in the 1150s although most of the present structure dates from the fourteenth century. The church was originally formed of the ancient rectories belonging to St. Peter’s Hospital which were joined together. The church was unfortunate enough to have been situated next to the city’s largest dung heap for many centuries.
The church remains standing today and contains a reset Norman doorway which was taken from St. Nicholas in Lawrence Street in the seventeenth century following damage to that church in the Civil War. The brick tower of St. Margaret’s was built between 1684 and 1685, using funds provided by the Archbishop of York, as the previous tower had collapsed during a storm in 1672.
In 1851 the north aisle was rebuilt and much of the church restored as part of a series of Victorian modernisations and restorations across York’s churches.
In 1955 the parish was incorporated into St. Denys’s and then closed. Today the building is now used by National Centre for Early Music, after having been used for a while by York Theatre as a prop store.