Among the churches of Kovrov, the Christ the Savior Cathedral is the oldest. There is a legend about its foundation. According to the legend, Prince Andrei Bogolyubsky got lost in these parts on the eve of Christmas. He was returning from Suzdal to Starodub and lost his way in the forest. The day was snowy and frosty, and it was already beginning to get dark when he noticed a faint light in the distance. It was a candle in the hunter Elifan's hut. The prince spent the night there, and the next day, in gratitude for his salvation, he ordered a church to be built in the village. The wooden church was consecrated in honor of the Nativity of Christ, as the event took place on the eve of this holiday.

In the late 17th century, the wooden church was replaced by a stone one. Initially, the church had two altars: the main one in honor of the Nativity of Jesus Christ and a side altar in the name of Macarius of Kaluga the Miracle Worker. Later, the church acquired the icon of the Mother of God "Smolensk," which became the main shrine of the cathedral. A new side altar was established in honor of this icon. According to legend, the icon was miraculously found intact on the ashes of a burned wooden church in the village of Nesterovo, 7 versts from Kovrov. Considering it miraculous, the icon was transferred to the Christ the Savior Cathedral.

In 1837, the church was attended by the Tsarevich Alexander Nikolaevich, the future Emperor Alexander II, and his mentor, the poet V. A. Zhukovsky, during a service. This was the only visit to the church by a high-ranking person. In 1870, the church was expanded and received the status of a cathedral. By that time, a watchman's lodge and a fence with gates had appeared.

From 1920 to 1926, the cathedral served as the cathedral for the Kovrov vicar of the Vladimir Archbishop. Archpriest Pavel Avrorov was the representative from the Vladimir diocese in the Supreme Church Administration, the central body of the renovationist movement, since 1922. However, most believers attended the Christ the Savior Cathedral, which belonged to the Old Church direction. In early 1926, an independent church community arose in Kovrov, opposing the extremes of the Tikhonist and renovationist churches. As a result of conflicts, the Christ the Savior Cathedral was assigned to the Old Church community, the Spaso-Preobrazhensky Cathedral to the renovationists, and the Church of John the Warrior to the autocephalists. In 1931, the authorities closed the Spaso-Preobrazhensky Cathedral, and in 1938, the Christ the Savior Cathedral, dismantling the roof of the church and the bell tower. The Church of John the Warrior remained with the renovationist community, but not for long. In 1945, it was also closed.

In 1946, the cathedral was reopened, restoring the roof in a simplified form. It was renovated in the late 1980s and remained the only functioning church in Kovrov until 1991.