The first Anglican Church was built about 1625 by the Levant Company for the use of its employees and other British residents of Smyrna. There has been an unbroken line of Chaplains resident in Izmir since 1630.

The current church, built for the use of British inhabitants and forming part of the premises of the British Consulate General was consecrated in 1900, and dedicated to St. John the Evangelist. For a long time now, the congregation of St John's has been international. It currently includes people from Iran, the USA, South America, France, Korea, Columbia, Kenya and the UK. The main common denominator is language (English!), rather than nationality or church tradition.

Bishop William Collins (Bishop of Gibraltar in Europe (1904-1911)) is buried beneath the west end of the church. Bishop Collins died on board the SS Saghalien, whilst on his way from Constantinople to a liturgy of Confirmation at St John's, on 22 March 1911.

Bishop Collins Memorial Hall, which adjoins the church was built in memory of the bishop. His episcopal ring was set into a beautiful silver chalice which is still used on special celebrations of the Eucharist.

St John's Church occupies a fine and prominent site close to the main Alsancak Gar (railway station). The former chaplain's residence is currently used by the British Foreign Office as its Consulate in Izmir. The current chaplain lives in an apartment close to the church.