On June 2, 1890, priest Vasily Koblov from the Kardailovskaya stanitsa was appointed the first rector of the new church. On September 30, 1890, on the eve of the Feast of the Protection of the Mother of God, Bishop Makary of Orenburg and Ural consecrated the third church in the new settlement of Orenburg, dedicated to the holy great martyr Dimitri of Thessalonica, in the presence of a large number of believers.

Over time, it became clear that the church was too small and needed expansion. In 1895, the Orenburg diocesan architect developed a project with two extensions for the altars, but due to a lack of funds, the implementation was delayed. Thanks to donations from parishioners and benefactors, including merchant of the 2nd guild Maxim Makeev, the right chapel in honor of the Holy Trinity was built and consecrated on August 1, 1899. In 1900, the construction of the left chapel in honor of the Dormition of the Mother of God was completed with funds from Major General Cherekhov and Makeev, who became the church elder. The rector of the church, Archpriest Alexander Slovokhotov, appealed to Bishop Vladimir with a request to consecrate the altar on August 13, 1900.

In the 1920s, the Dimitri Church was handed over to the Renovationist community due to non-fulfillment of the contract conditions. In the 1930s, the church was used by two communities: the 'Old Church' and the Renovationists. In 1933, the church was closed, but reopened in 1935, and after the closure of the Kazan Cathedral, the archbishop's see was moved here. However, the Orthodox only had the left chapel, while the central and right remained with the Renovationists. On September 17, 1938, the church was finally closed, and in January 1939, the building was handed over to Oblkinotrest for conversion into a cinema.

During the Great Patriotic War, an automotive company of the South Ural district was located on the church's territory. On January 5, 1944, believers appealed to the city council with a request to reopen the church, but were denied due to the occupancy of the premises. Subsequent appeals in 1944 and 1946 were also rejected, despite the fact that the company had vacated the territory. Later, the 'Burevestnik' cinema opened here, operating for more than half a century.

In August 1989, a group of believers registered a new religious society of the Russian Orthodox Church in the Central District Executive Committee of Orenburg. On September 27, 1989, the Council for Religious Affairs allowed the society to acquire a residential building for prayer purposes. On February 12, 1990, the building of the former Dimitri Church was returned to the Orthodox Church.

On February 27, 1996, a dome was installed on the church with a large gathering of parishioners and residents of Popov and Ostrovsky streets. By November 1999, the Tabyn icon of the Mother of God and the icon of St. Dimitri of Thessalonica were brought to the church. Later, the construction of the bell tower was completed, and on August 16, 1999, Metropolitan Valentin of Orenburg and Buzuluk served a prayer for its opening.