The church dedicated to the icon of the Mother of God "Smolensk", with a warm chapel in honor of Saint Catherine the Great Martyr, was built with the funds of Murom merchant M. I. Elin on the site of a wooden church that burned down in 1804.

In 1832, a bell tower was added to the church, and in 1838, a warm refectory with a chapel in honor of the icon of the Mother of God "Joy of All Who Sorrow" was attached, uniting the bell tower and the church into a single complex. The architecture of the church and bell tower reflects the influence of the era of Emperor Alexander I.

In 1840, parishioners, among whom were Murom merchants Titov, Elin, and Kiselev, donated a bell weighing 200 poods. A special relic of the church was considered to be the altar cross from 1676 with particles of holy relics.

After the collapse of the spire of the neighboring Church of Cosmas and Damian in 1868, the surviving icons and church utensils were transferred to the Smolensk temple, which became known as the "New-Cosmodemyansk" church.

On May 23, 1922, silver utensils weighing 1 pood, 19 pounds, and 80 zolotniks were confiscated from the church under the pretext of helping the starving in the Volga region. On November 12, 1929, the closure of the church was discussed, and on January 20, 1930, the All-Russian Central Executive Committee approved the decision to close eight churches in Murom, including the Smolensk one.

Since 1977, restoration work began in the church, after which it became an exhibition hall for the local museum of local lore. Exhibitions of fine and applied arts, as well as concerts of academic choirs, were held here due to the excellent acoustics.

On July 21, 1995, lightning struck the spire of the bell tower, causing a fire and collapse. In August 1995, the church was returned to the Vladimir diocese, and the first service was held on August 10. The first Easter service was conducted by Archimandrite Kronid Kozlov on April 14, 1996.

In August 2000, the spire of the bell tower, damaged by the lightning strike, was restored. By the decree of Archbishop Evlogy Smirnov, the church was granted the status of a city cathedral.

The main volume of the church is a square with a vaulted ceiling, crowned with two octagons that decrease in diameter, topped with an onion-shaped dome. A five-sided apse adjoins from the east, while from the north and south, there are porticos of the Ionic order with arches, creating an impression of lightness.

The refectory and bell tower, built in the 1830s, are executed in different scales and are somewhat disproportionate to the main volume of the church. The architectural details are characteristic of the first half of the 18th century: arched windows of the refectory, pilasters of the entrance portico, and half-columns of the third tier of the bell tower. In the third tier, three half-columns of the composite order are grouped together, which is a local tradition of the builders known as "Murols."