The story of St John's Church buildings began around the year 1892. At that time the land on which the church stands was an empty plot, and new residential housing was being developed under the title of New Cherry Hinton within the area between Hills Road and Cherry Hinton Road. A committee of town and University people, under the chair of the Master of Peterhouse, was formed in 1891 with the purpose of raising funds for building a new church. The plot was acquired, and a small wooden schoolroom was erected to serve as the premises for a Sunday School. The new congregation first met in the chapel of Homerton College (then called Cavendish College).
By May 1896 fund-raising had reached the point whereby the foundation stone could be laid, and by the end of the year the Eastern half of the present church building had been completed. This consisted of the chancel and two bays of the nave. In order to be able to start to use the part of the building that had been built for services, the West end was blocked off by a wall made from yellow Cambridge bricks. The architects were Gordon, Lowther and Gunton.
The next stage in the building was the construction of the vestries for the clergy and choir in 1909. Progress was then stalled by the Great War of 1914–18. After the war efforts were renewed to raise the funds required for the church to be extended to the size of the original plans, and by 1929 it was possible to complete the building, at least to a revised design. The original plans had included a tower and spire; those who worry about church finances today are relieved that these were dropped from the final plan!
Subsequent to the completion of the church was the development of the community rooms on the South side of the church. The original community room was built in 1982, and later extended, with the provision of a new entrance area, in 1995.