The church was consecrated in 1838. Externally, it looks like a one-story rotunda with four two-column porticos arranged in a cross shape. The church at the cemetery was built at the initiative of titular advisor Dmitry Voinov, and its interior decoration was created by his son, collegiate advisor Matvey Voinov.

Since 1839, the All Saints Church was attached to the Tyumen Protection Church. There was no regular clergy, except for the elder who took care of the church. Services were held rarely. In 1884, the cemetery where the church was located was closed for burials and remained unattended for a long time, subject to plundering. Order was restored only in 1908.

With the advent of Soviet power and after the decree of 1918 on the separation of church and state, the Church of All Saints, like other religious institutions, had to register as a religious community. During the anti-religious persecutions, more than 12 kg of silver utensils and two bells weighing 96 kg were confiscated from the church.

In 1930, all cult buildings in Tyumen, except for the All Saints Church, were closed. The church was planned to be converted into a school, but these plans did not materialize, and the church continued to function, remaining the only place for communal prayer in the city.

The first church elder under Soviet power was Andrei Grigorievich Boyarintsev, and the church council was headed by archpriest Nikolai Protopopov. During the period of repression, Father Nikolai and his wife Lukiya were deprived of their voting rights, and Nikolai himself was arrested and repressed, dying in 1932. In 1989, he was posthumously rehabilitated. From 1933 to 1937, the community was led by Mikhail Yakovlevich Khangin, and the priest was Father Dioscor Tatiyshev. Both were convicted and executed.

During the years of the 'Yezhovshchina', the church faced pressure from renovators and was closed from 1940 to October 1941. Externally, it was almost undamaged, but the cross was removed. In early 1942, services were allowed to resume, a cross was made at the factory and installed for the Feast of the Baptism. An iconostasis from the destroyed church of the village of Zavodouspenka was installed in the temple. During the war, funds collected in the church were distributed to the front, for the restoration of the church, and other needs.

The first organizer of the church's restoration was priest Alexander Syuchugov, who later became its rector. The church also hosted Father Nikifor and igumen Ignaty, who had undergone exile and hard labor. In the 1940s-1950s, priest Matvey Pakhomov served, awarded for his diligent service. After the war, the rectors included archpriests Trofim Goncharov, Ioann Shiprikovich, Alexander Kuznetsov, and others.

In the 1980s, a stone annex with a baptistery was built, where the first immersion baptismal font in Tyumen appeared. A place for selling candles and church utensils was also set up here. In 2002, the annex was recognized as corresponding to the style of church classicism. A prosphora room, vestment room, and laundry were built.

As part of the preparations for the millennium of the Baptism of Rus, repair work was carried out in the church. Igumen Evtiy Kurachkin initiated the restoration and replacement of the iconostasis. A new iconostasis was made in Omsk, and the old one was transported to the Abalak Monastery. The roof of the church was also replaced, and a new cross was installed.

In 1997, a children's Sunday school and library were opened in the church. In 2004, the construction of the bell tower was completed, where a Youth Center began operating.

In January 2000, the church was assigned to care for the church of Saint Catherine the Great Martyr in the village of Sozonovo. Since 2006, the church of Saint Prince Alexander Nevsky at the Tyumen Law Institute of the Ministry of Internal Affairs of Russia has been attached to the church, and since 2007, the church of Saint Prince Dmitry Donskoy.