Stony Stratford has a long history of welcoming travellers because of its location straddling the Roman road which ran from London to Chester, now the A5. The Watling Street also marked the boundary between the ancient manors of Calverton to the west and Wolverton to the east. Both manors provided chapels of ease in the town which were later replaced by churches dedicated respectively to St Giles and St Mary Magdalen.
On 6th May 1742 a fire started in The Bull Hotel and spread through the town destroying 146 buildings including St Mary's church. Only the tower survives today. After the fire it was decided to rebuild and enlarge the church of St Giles. The 15th century tower was retained and to this was added the nave we see today with its slender fluted columns and vaulted ceiling with plaster ribbed groins.
The rebuilding included a gallery to increase the seating capacity and was completed in 1777 in the architectural style known as 'Strawberry Hill Gothic'. The Victorian era saw the addition of vestries, the installation of a Gothic chancel screen, stained glass memorial windows, and a Lady Chapel created in the southeast corner of the nave.
A fire in the church on Boxing Day 1964 resulted in the organ being completely destroyed and the church severely damaged by smoke. Services continued in the smaller church of St Mary the Virgin in London Road until St Giles could be reordered and decorated. When the church of St Mary the Virgin was closed the two parishes were combined and on Palm Sunday, 7th April 1968 St Giles church was reconsecrated as the church of St Mary & St Giles