The Pokrovsky Church was built in Krasnoyarsk at the beginning of stone construction after a major fire that destroyed a significant part of the city. Earlier stone structures have not survived, so the church is considered the oldest stone building in the city. The first wooden church in honor of the Protection of the Holy Virgin appeared in Krasnoyarsk in the mid-17th century, shortly after the establishment of the fort. It was located not far from the current church. The wooden church burned down several times and was rebuilt as the city continued to grow. The fire of 1773 was particularly devastating, destroying entire neighborhoods with residential houses, stone buildings, and churches. After this, it was decided to build key buildings from stone for better fire protection. Stone construction in Krasnoyarsk began a little earlier, with the foundation of the Resurrection Cathedral laid in 1759, which took more than ten years to build. The slow pace can be explained by the fact that stone architecture in Eastern Siberia was a novelty, and there were few craftsmen. The cathedral was built by stonemasons from Yeniseisk, but specialists were still lacking. Understanding that the stone Pokrovsky Church would take a long time to wait for, the parishioners asked Archbishop Varlaam Petrov of Tobolsk for permission to build a temporary wooden church, which would later be replaced by a stone one. The archbishop agreed, and the church was built. The stone church was only laid in 1785 and completed ten years later, almost a quarter of a century after the fire.

The wooden Pokrovskaya church had an unusual fate. In 1790, after the consecration of the chapels of the stone church, it was moved and consecrated in honor of the Annunciation of the Holy Virgin. Later it was moved again and consecrated, now it became All Saints. The church could have been moved a third time, but it burned down, serving as a prototype for three stone churches in Krasnoyarsk. It is known that it was a tent-like church with a refectory and a bell tower on one axis. The stone Pokrovsky Church was built next to the wooden one. Funds for construction were collected from all over, many helped not only with money but also with labor. The work was led by retired nobleman Mikhail Yushkov, who was considered the chief architect of the church, although it was more of a collective creation. Yushkov and the church elder Daniil Cherkasov were most concerned with staffing, as Krasnoyarsk was entirely wooden, and there were no stonemasons in the city. Craftsmen were brought in from Yeniseisk, where stone construction was already underway. The construction progressed slowly, and in 1790 the side Peter and Paul chapel was consecrated, followed by the Nikolsky chapel. At that time, the wooden church was moved, and the parish "relocated" to the new church. It took another five years to complete the work, and the main altar was consecrated in June 1795. Initially, it was intended to be named Epiphany, but the parish vote designated it as Pokrovsky. The church was famous for its carved iconostasis, made by Fyodor Ushakov, which was preserved until the mid-19th century. The appearance of the Pokrovsky Church initially differed from the modern one.

According to the clerical report of 1813, it was a one-story church with two chapels and a bell tower, made of stone, with length and width measured in fathoms. In 1826, the wooden fence was replaced with a stone one with wooden grilles, which later became iron. Initially, the western facade of the entire church was the facade of the bell tower with a covered stone porch. In the 1840s, the porch was dismantled, a narthex was arranged, and the refectory was expanded, surrounding the bell tower. The new extensions were decorated, imitating the details of the original volume, and it is difficult to determine the boundary between the old and new parts of the walls. The old walls were plastered, and outdoor frescoes appeared, which were destroyed in the fire of 1881. After the church was expanded, all nine domes were gilded. In the 19th century, the church was painted, but only one fragment depicting the Protection of the Holy Virgin has survived. The other paintings were painted over in the mid-20th century. In 1845, the old iconostasis was sold, and a new gilded one took its place. In 1871, the church was expanded as space became insufficient. Merchant N. Gadalov donated over 10,000 rubles for the work, which progressed quickly. The church became more spacious, and a new icon of the Protection of the Holy Virgin appeared above the entrance.

Many churches in Siberia were closed later than in Central Russia, where the assault on religion began in 1918. In 1922, a decision was made to confiscate church valuables, and the authorities of Krasnoyarsk began to implement it. In May, they reached the Pokrovsky Church, where more than 23 poods of silver were confiscated. Despite the looting, the church remained active for more than ten years. In 1935, it was closed and transferred to the city communal services. By the beginning of the Great Patriotic War, there were no functioning churches left in the Krasnoyarsk diocese. In 1944, after a letter from the faithful, the authorities allowed the Pokrovsky Church to reopen. The believers restored the church, and it opened on May 8, 1945, becoming the main church of the diocese.

In the 1950s, the interior of the church changed significantly. The wall paintings were covered with plaster, decorated with stucco featuring plant ornamentation. The stucco elements look unusual but beautiful, framing the icons and vaults. In 1961, the Pokrovsky Cathedral was closed again. The cemetery Trinity Church remained active, while the cathedral was used as workshops and an exhibition hall. In 1989, the church was returned to the faithful. The Pokrovsky Church belongs to the Yenisei school of Siberian Baroque. The height of the church with the cross is 32 meters, the bell tower is 36 meters. The length along the central axis is over 40 meters. The bell tower has 10 bells, and there is a staircase leading to it. There are utility buildings near the church, one of which houses a small consecrated baptismal chapel. The church is topped with nine domes.