The church was originally wooden and located on the territory of the Assumption Monastery, which was dissolved in 1626. It was founded in 1622 by the first Tobolsk archbishop Cyprian.

Over time, the temple deteriorated due to frequent fires, and it was decided to rebuild it. In 1789, Yegor Domonevsky and Pyotr Baranov laid the stone foundation of the church, although the construction is often attributed to Ivan Karpov and Ivan Nedomolvin. The work was completed in 1807.

In the late 19th century, the cold upper floor was converted into a warm one with funds from parishioners P. B. Shumilov and A. E. Kukhtorin. In 1897, a 16-ton bell, cast at the initiative of Andrey Afanasyevich Vasilyev, was raised to a separate bell tower.

In 1922, by the act of the provincial commission, part of the silver utensils, including crosses, candlesticks, a censer, and lamps, were confiscated from the church. In 1930, the church bell was removed and melted down.

In August 1936, the church was closed, but it was reopened 21 days later at the request of parishioners. However, it was closed again in October. In 1937, the demolition of the church was planned, but in the end, only the fence was removed.

In the 1930s, the church building housed the State Construction Trust (courses and dormitory for workers), a garage for vehicles, and later a grain storage. In the 1940s, archives of the RSFSR for the Far East were moved to the church due to fears of a Japanese invasion of the USSR.

In the 1980s and 1990s, the facades of the building were restored, the altars were repaired, the framework of the iconostasis, domes, and roof were restored, as well as the gilded crosses. In 2004, a copy of the famous bell was installed on the newly built bell tower.