The church of St John the Evangelist was founded in 1891 as the Cambridge residential area extended south of the city into the land between Hills Road and Cherry Hinton Road. In the early days it had neither building nor clergy. The first congregation met in the chapel of Homerton College (then called Cavendish College). St John's was founded as the daughter church of St Andrew's church, Cherry Hinton, but the distance from St Andrew's (2.5 miles) meant that the services were normally led by local clergy or chaplains from the University colleges.

In the early days, the efforts to establish the church and raise funds for a building were undertaken by a committee with members drawn from the local community and the University of Cambridge, under the chair of the Master of Peterhouse. After only a short while a retired clergyman, the Reverend John George, offered to serve as curate-in-change on a voluntary basis (1893). He played a significant role in the project to build the new church; he and his wife donated the pulpit to mark their silver wedding anniversary. The first stage of the church building was made usable by the end of 1897, and Rev George became St John's first vicar that year. He served until 1903; a plaque on the chancel wall commemorates the work of the Rev George, and two stained-glass windows in the chancel were given in memory of the Rev George and his wife Edith.

The second vicar, Reverend Love, served 11 years (1903–1914), and oversaw the building of the the choir and clergy vestries (1909). He was followed by Reverend Jackson (1914–1927), who oversaw the building of the Parish Hall on the corner of Blinco Grove and Baldock Way, which served as the base for the Sunday School. This period overlapped the tragedy of Great War, which saw the death of 45 parishioners in service in the armed forces. In spite of the war, efforts to raise funds for the building of the church continued, and it was possible to complete the extension of the west half of the church in 1929 during the priesthood of Reverend Patterson Morgan (1927–1938). The tragedy of the Second World War occurred during the priesthood of Reverend Robert Jary (1938–1947), and the church served the local community and the forces in a number of ways. A period of consolidation of parish work, particularly with young people, followed during the priesthoods of Reverend John Needham (1947–1955) during which time the organ was installed, and Canon Frederick Stanbury (1956–1974). During the priesthood of Canon Frederick Wilkinson (1975–1988) a new parish room was built on the South side of the church, which was extended during the time of his successor, Canon Brian Jones (1989–1997). This marked the end of the building of the church. Canons David Reindorp (1997–2006) and Susan Wyatt (2006–June 2016) have subsequently led St John's in further establishing the work of St John's in the local area.

Over the years St John's has been fortunate to have had a number of wonderful curates and honorary priests. Some of these have gained national attention. One curate, Stephen Sykes (1985–2006) was Regius Professor of Divinity at the University of Cambridge, and subsequently served as Bishop of Ely. Before being ordained as Vicar of St Bene't's in Cambridge, the Reverend Angela Tilby served as honorary priest from 1997–2006; Angela is well-known for her work on BBC Radio 4, particularly as a regular contributor to Thought for the Day and the Morning Service. A previous vicar, Reverend Canon David Reindorp, was chaplain on the television series Lad's Army and other reality-style programmes.