St. John’s church was built by John Coppin, who lived at Markyate Cell, as a Chapel of Ease in 1734 for the people of Markyate who previously had to travel to one of the three parishes of Caddington, Flamstead and Studham (Humbershoe). Built of brick it consisted of the nave measuring 48 x 18 feet with an entrance on the north side reached by a flight of steps.
The interior had a flat ceiling, a ‘three decker’ pulpit (for clerk, reader and Vicar, respectively), and box pews with fireplaces for the founder’s use. The tower at the west end was built soon after, possibly in 1735, when the gallery was constructed across the nave to house the choir and musicians with access from stairs within the tower.
Over the years north and south aisles were built by incumbents of Markyate Cell with new stairs to the gallery, the ceiling removed and the underside of the roof match-boarded.
In 1877 an ecclesiastical district of Markyate was founded and St. John’s became the parochial church authorised to solemnise marriages, churchings and baptisms and the incumbent was to be known as the Vicar. The chancel was eventually built in 1892 after many attempts to raise the necessary funds.
The 20th Century saw a new organ installed, given by the widow of Rev. Francis Adye in his memory. The east window was replaced in 1919 and is dedicated to the memory of Col. J.S. Collings-Wells, V.C., D.S.O. and men of Markyate who fell in WW1. Also, towards the end of the century a kitchen, toilet and new room for choir robing were built.
In the 21st Century a sound system and under seat heating have been installed. The Chancel Roof has been repaired and major repairs to the organ have been completed.