In 1789, a stone two-story church with a bell tower and two altars was built on the left bank of the Tura River in Tyumen, funded by parishioners: the upper floor in honor of the Ascension of the Lord, and the lower one in the name of St. George the Great Martyr.

In 1870, thanks to the will of Tyumen merchant I.V. Okonishnikov, a chapel in honor of the Transfiguration of the Lord was added to the church on the right side. In the same year, merchant of the 1st guild E.A. Kotovshchikov donated funds for the construction of a chapel on the left side, dedicated to the Nativity of the Most Holy Theotokos.

The Ascension Church was associated with a wooden chapel in the name of the Holy Apostles Peter and Paul in the village of Yar, a church in honor of the icon of the Most Holy Theotokos “Joy of All Who Sorrow” in the village of Mys, and the Three Saints Church at the Zarechny Cemetery in Tyumen.

In 1929, the Ascension-St. George Church was closed, and its building was repurposed as a club for tanners and chemists. From 1934 to 1935, the building housed a dormitory for students of the drivers and combine operators school of the Tyumen Agricultural Technical School. Later, the building was managed by the Tyumen sheepskin and fur factory.

On July 5, 1976, the church building was recognized as a monument of history and culture of local significance. In 1996, it was transferred to the Tobolsk-Tyumen Diocese, and regular services resumed in the temple in March 2001.

In 2003, work began on restoring the lost bell tower, completed in 2005. That same year, a dome was installed, bells were raised, the heating system was updated, the building was insulated, and the first-floor windows were replaced with plastic ones. All work was funded by benefactors. In September 2006, the church and Sunday school were gasified with funds from the city budget.

On October 21, 2006, a significant event occurred for the parish and the Russian Orthodox Church: the relics of the enlightener of Siberia, Metropolitan Filofey Leshchinsky of Tobolsk, were discovered. He served in Siberia for 25 years and bequeathed to be buried outside the church in the Tyumen Holy Trinity Monastery. After the monastery was closed, his remains were secretly reburied in the Ascension-St. George Church. It was officially believed that the relics had been destroyed, as claimed by the Bolshevik press.

The story of the discovery of the relics began in 2003 when a woman informed the abbot of the Trinity Monastery, Archimandrite Tikhon Bobov, about the burial place of the saint. It turned out that she was the daughter of Archpriest Alexander Syuchugov, who left a will for Filofey to be buried by the left column of the church. By the blessing of Archbishop Dmitry of Tobolsk and Tyumen, a commission was formed, which after several attempts found the relics and transferred them to the Holy Trinity Monastery.

In 2006, the church was included in the regional program for the restoration of architectural monuments. Funds were allocated for the development of a reconstruction project, foundation strengthening work was carried out, and project and estimate documentation was created. Restoration continues to this day.