In the early years of the 20th Century, Anglicans living in Asquith, Mount Colah and Mount Kuring-gai had to make the trip to St Peters in Hornsby (established 1898) if they wished to worship together in a church building. The alternative was occasional services, which were held in the homes of local parishioners in both Asquith and Mount Colah.

Around 1919, as the population continued to grow, the people of the area decided it was time they had their own church building, where they could hold services and start a Sunday School. A group of interested residents met with the Rector of the Parish of Hornsby (which at that time extended from Waitara to Brooklyn). Mount Colah was ruled out as a location for a new church, and so other options were considered.

A new estate at Asquith was being opened up; and so with 90 pounds raised from various events, and the help of the Home Mission Society (which lent them the balance needed), two blocks of land were acquired.

The church building was constructed entirely by volunteer labour; the funds needed for materials being raised by parishioners. Seating and an organ were purchased second hand, and books and a bell were presented to the new church as gifts. The first Sunday School was held at St John's on the 1st May 1923, with 40 to 50 students attending.

Occasional services continued to be held at parishioners' homes in Mount Colah and Mount Kuring-gai, and in 1939 these became regular events (alternate Sundays each month at 3pm), until St Georges in Mount Colah was opened in 1946 and Holy Trinity Mount Kuring-gai opened in 1954.

Services were held in both churches until Holy Trinity was resumed by the Government in 1985 to make way for the F3 Freeway, and St Georges was closed in 1991 (and demolished in 2007) because there was no possibility of further expansion on the difficult site. Some proceeds from both properties were used to build the new (third generation) church at Asquith in 2004. The second generation church (now in use as a Church Hall) was commissioned in 1969 and decommissioned in 2004.

In August 2007, the property adjacent to St John's (#8 Royston Parade) was purchased from the Catholic Church. In previous years, the large rambling house at #8 had been used as a refuge for troubled youth. It will be demolished to make way for two new dwellings to be used for ministry housing. The old rectory at #4 Royston Parade was sold in order to fund the new houses at #8.