In 1949, a group of young people who came to Canada for contract work approached Father Georgy Burdikov in Windsor for help in establishing an Orthodox church. At that time, Father Georgy was the dean and contacted Jordanville, from where Priest Nikolai Martyshevsky was sent. On Christmas in 1950, the first Orthodox service was held at St. Paul's Anglican Cathedral. The parish began to develop in a rented space on the second floor at 212 Dundas St., where the first church holiday was celebrated. In the early 1950s, Russians, Ukrainians, Belarusians, Serbs, Syrians, and Greeks joined the parish.

They decided to build a new church by their own efforts, trying to preserve Russian Orthodox traditions in architecture. The project by Alexander Vladimirovich Zauer won the competition. The construction was overseen by engineer D. D. Polyakov from Toronto, who developed the complete construction project for free.

On October 18, 1958, His Grace Vitaly, Bishop of Montreal and Canada, consecrated the laying of the foundation, and on October 25, 1958, the cornerstone of the altar wall was consecrated and laid. By the winter of 1959, the basement walls and ceiling were erected. A church was arranged in the basement, and the first Easter in the new church was celebrated in the spring of 1959.

In 1964, the church was solemnly consecrated by His Grace Vitaly, with the participation of the clergy and a large number of guests. Currently, services are conducted in Church Slavonic and once a month in English.

It is important to mention that prior to this, the Transfiguration parish of the Russian Orthodox Church had been operating in London, Canada, since 1916 under the omophorion of Bishop Alexander (Nemolovsky) of North America and the Aleutians. By 1917, the parish had built a church where priests from Russia served. However, after the revolution, the church was sold, and the building became a Russian film club. It is now privately owned on Leard St.