The church was founded in April 1972 as a parish of the Orthodox Church in America. This happened thanks to Archpriest Grigory Malyshev and other Russian migrants who transitioned to the OCA from the Russian Orthodox Church Outside Russia. To meet the needs of the parishioners at that time, services were conducted in Church Slavonic. Initially, services were held in homes, and in 1974, a house was purchased and transformed into a church.

After the Russian Orthodox Church Outside Russia united with the Moscow Patriarchate, the Annunciation parish in Brisbane came under the administration of the American Orthodox Church, remaining under the omophorion of the Russian Abroad Church. Father John Weir was appointed as the rector and began conducting services in May 2009, actively strengthening the parish: he performed services, carried out renovations, and trained the choir.

In early 2010, Father Mikhail Klebansky became the rector. In July 2010, Father Alexander Borodin was appointed to this position, ensuring long-term stability for the parish. Church supplies were acquired, a ramp for the disabled was installed, and the interior of the church was expanded. Education became a priority, with catechism and Bible study courses organized.

In 2015, the parish began conducting services for a small community of Orthodox Christians in Toowoomba, which later became the mission of St. John.

In August 2017, Father Andrew Smith was appointed as the rector, who serves to this day.

Currently, the parish is the only permanent English-speaking Orthodox parish in Brisbane and one of the few in Australia.