On May 1, 1774, at the request of the residents of Yeniseisk and with the blessing of Archbishop Varlaam of Tobolsk and Siberia, the wooden church in the Gostiny Dvor, known as the Znamenskaya, was moved to the cemetery outside the city. This was due to the beginning of the construction of a stone church in its place. In 1774, the church was consecrated in honor of the Assumption of the Mother of God. Over time, its wooden structure deteriorated and was dismantled to make way for a new brick building.

On September 9, 1793, with the blessing of Archbishop Varlaam and with funds from merchant Yefim Treskin, a new stone cemetery church of the Assumption was laid. On August 27, 1794, merchant Pyotr Treskin laid the second floor of the building. By 1799, the construction of the lower floor was completed, and on July 11 of the same year, the church was consecrated. The chapel of the upper floor was consecrated on July 17, 1818, in honor of the holy apostles Peter and Paul.

In 1826, Bishop Mikhail of Irkutsk laid a warm chapel on the northern side, which was consecrated on November 23, 1827, in the name of St. Innocent of Irkutsk. The chapel was built with funds from merchant Alexander Kobichev. On August 25, 1843, the second chapel on the second floor was consecrated in honor of Saint Prince Alexander Nevsky, built with funds from Alexander Alexandrovich Kobichev.

Until 1823, the Assumption Church was a subsidiary cemetery church. Its architecture, although somewhat austere, corresponds to the all-Russian traditions of that time with elements of Siberian Baroque. The church has a massive bell tower with a spire and cross, five domes, and two over the altars.

In 1923, the first wave of church closures began in Yeniseisk. The Assumption Church was served by Archpriest Nikolai Pikanovsky, psalmist Vasily Bakshaev, and priest Ioann Vazinger. The lists of parishioners included 67 founders and 250 parishioners. On April 17, 1923, the church was handed over to the community of believers.

In the 1930s, the second wave of church closures began, and by the end of the decade, all churches in Yeniseisk were closed. Special settlers lived in the lower part of the Assumption Church, while the upper part housed an airport club. In 1937, priest Ioann Vazinger was shot, and the bell was removed from the church.

On July 3, 1946, the Assumption Church was handed over to the parish of the Orthodox Church. The first priest was Archpriest Evgeny Bobovsky. In 1950, the repair of the cathedral was completed, but the bell and domes were absent until 1988.

Since 1961, layman Ivan Pirozhenko became the chairman of the church council. In the 1980s, the authorities' attitude towards the church softened. In 1986, seven domes were installed on the temple, and the facade was restored. For the 1000th anniversary of the Baptism of Rus, an ancient bell was transferred to the church.

From 2016 to 2019, restoration work was carried out on the ensemble of the Assumption Church, including the installation of heating systems and the replacement of doors.