Even before the founding of the city, a fishing settlement known as "Simbirsk" was established on the banks of the Volga. By the mid-17th century, the Orthodox residents of this settlement had already built the Cathedral Church of the Smolensk Mother of God. The church was located on the Smolensky descent to the Volga, on the northern side of the city, on a steep slope, on a relatively flat area with a picturesque view of the Volga, surrounded by nature. The white stone church, resembling a ship, was dedicated to the Smolensk Icon of the Mother of God. The construction of the Smolensk church was carried out in stages. The oldest part is the cold church, located on the eastern side. Initially, the church was a skete or desert and belonged to the Assumption Monastery. During the siege and battles with the troops of Stepan Razin, the fortress of the city and the Smolensk church remained unharmed.

In 1674, after the construction of the Assumption church and the restoration of the Assumption Monastery, the Smolensk church separated from the monastery and became a parish church. Initially, it was maintained by a small parish and income from a chapel at the cemetery located near the Volga. By 1674, the Simbirsk Assumption Monastery included: the Assumption Monastery with the Assumption church, the Solovetsky desert located 17 versts north of Simbirsk on the right wooded bank of the Volga, and the Smolensk church. The Assumption church was dismantled in 1866 and moved to the hilly part of the city. The Solovetsky desert existed until 1764, while the Smolensk church lasted until the early 20th century.

In 1751, former Simbirsk merchant I.I. Vorontsov added a warm stone church of the same name to the existing cold stone church along the west-east axis. Both buildings were connected by a door arranged in the altar of the warm church, at the point of its connection with the western wall of the cold church. A three-tiered stone bell tower was built next to the warm church. Initially, both churches were covered with shingles, then with iron and painted with verdigris. The fence was wooden, but it disappeared in the 19th century.

In 1913, the temple was severely damaged due to a landslide, and in the late 1920s, it was closed due to its emergency condition. The Smolensk church was finally dismantled after 1932.