The history of the church is closely linked to the development of the village of Petropavlovsk, located near Shuya. The village began with a tragic event in 1831 when a cholera epidemic claimed many lives of local residents. The city cemeteries could not cope with the number of the deceased, so it was decided to create a separate burial site in the sparsely populated outskirts of the city, in the Ryokovo area. In memory of the cholera victims, the residents of Shuya established a procession with a week-long fast starting from July 28. The procession passed through the city center to the burial site, where a memorial service was held with the carrying of revered icons. The burial site was surrounded by an earthen mound, and in 1847, the city mayor I.D. Kiselev erected a white stone monument with an inscription about those who perished from cholera in 1831.

In the second half of the 19th century, the area began to be actively populated. This was due to the fact that the landowner, merchant G.V. Bolotov, rented it out, attracting residents from nearby villages who were seeking opportunities for work near the factory town of Shuya. The settlement grew, and the need for a church arose. In 1868, a chapel was built and consecrated on the site of the cholera burial, which later became a church. The construction was financed by the Shuya merchant G.V. Bolotov and the honorary citizen of Shuya M.I. Shchekoldina. After the church was built, the Ryokovo area was named the village of Petropavlovsk. Until 1876, the church was affiliated with the Resurrection Cathedral, but then it became a parish church thanks to funds found for maintaining a separate clergy.

By the end of the 19th century, it became clear that the old church did not meet the requirements for capacity and architecture, so it was decided to rebuild it. Thanks to the efforts of church elder E.A. Gusev, a new church was built on a new site from 1891 to 1893. The project was developed by Vladimir architect N.D. Koritsky. The church was built in the Russian style with elements of Ton's architecture. Inside, there was a cast-iron floor and a stove, and the iconostasis housed 20 icons on a golden background. The large bell weighed 160 poods. The church was handed over to the parish on January 30, 1996, and the first service took place on April 11 of the same year. In 2002, the iconostasis was restored, and since 2003, the relics of Saint Martyr Avksenty have been housed in the church. Currently, the church is actively being restored: a new fence and dome have been installed, repairs have been made, and the restoration of the bell tower is planned.