St Mary’s stands in the physical centre of the old walled City, and the university grew up around it. In medieval times scholars lived in houses with their teachers and the university had no buildings of its own, so it adopted St Mary’s as its centre. The church continued as a parish church, but by the early 13th century it had become the seat of university government, academic disputation, and the awarding of degrees.

By the 14th century, as colleges were beginning to be founded, the expanding university, desperately in need of more room for its business, constructed the Old Congregation House (c.1320), a small building of two storeys, on the north-east side of the church, abutting the tower. The House was built with money left by Bishop Cobham for that purpose, and to house his books. Thus the upper room became the first university library, containing a small number of chained books, and also the place where the university’s money was kept in the university chest. The lower room, which now houses the cafe, was used by the university’s ‘parliament’.

All university business was removed from the church by the middle of the 17th century, but St Mary’s remains the place where the university formally comes to worship. On two Sundays during term time, the formal university sermon is preached here, before the vice-chancellor and proctors, who enter with full ceremonial procession to their throne-like seats at the back of the nave.

The present pulpit and furnishings were installed by the University in 1827. Galleries were erected on the north and west walls, creating in the nave an auditorium which could seat a huge congregation.