The Peter and Paul Church of the Holy Trinity Monastery was founded in 1726 during the lifetime of Saint Philotheus, the Metropolitan of Tobolsk, by the southern wall. The inspiration for the construction was the church at the economic gates of the Kiev-Pechersk Lavra. Saint Philotheus aimed to immortalize the name day of Emperor Peter, whom he deeply respected. The emperor also honored the great Siberian saint.

Construction of the church began only in 1733. In the monastery's cathedral book, which is preserved in the archives, there are appeals from the church hierarchy to the residents of Tyumen requesting donations for the completion of the stone church, known as the Twelve Apostles, as well as for the construction of the bell tower and fence. These works were initiated by the efforts and funds of Saint Philotheus, the Metropolitan of Tobolsk and Siberia.

Construction resumed thanks to donations, but in 1736 it was halted as most of the stonemasons were sent beyond the Urals for other work by the Siberian provincial office. Archimandrite Zinovy complained to Metropolitan Antoniy Stakhovsky, accusing Foma Felisov of depriving the monastery of builders, but the craftsmen could not be returned.

In 1760, the church was combined with the bell tower and a one-story sacristy and two-story spiritual administration building. In 1770, a second floor was added to the sacristy. The Peter and Paul Church was consecrated on August 30, 1755, by the decree of Metropolitan Silvester Golovatovsky. The five-domed Peter and Paul Church, about 36.56 m tall and 22 m wide, was often referred to as cross-shaped due to its form resembling an equilateral cross. After the completion of construction in 1775, no major stone works were carried out in the monastery, only repairs and updates of existing buildings.

In 1842, a major fire occurred in Tyumen, destroying about 200 houses near the monastery. The Peter and Paul Church was so severely damaged that only the stone walls remained. The monastery's abbot, Archimandrite Vladimir, conducted a major renovation of both the Peter and Paul Church and the Trinity Cathedral with donations from benefactors.

In 1923, the Peter and Paul Church was closed. From 1934, the building was under the jurisdiction of the People's Commissariat. In 1960, it housed workshops of the art fund and branches of the regional local history museum.

On August 19, 2003, the church was transferred to the Tobolsk-Tyumen Diocese. Currently, services are held in the church.