The Resurrection Church on Debra is the only surviving urban temple of the 17th century in Kostroma. It was built in the mid-17th century, no later than 1652.

Lower Debra, one of the oldest streets in Kostroma, is located along the left bank of the Volga. The name of the street is associated with the dense thickets by the river and the wooded lowland. This version is confirmed by the name of the neighboring street, Forest. However, by the 17th century, the name Lower Debra competed with another, Lower Embankment Street, and from the second half of the 19th century, Lower Quay Street.

According to legend, the first church "on the lower debra" was built by the Kostroma prince Vasily Yaroslavich. His "Life" states that the young prince loved to hunt in the forests above the Black River and, to avoid transporting dogs from Sula, moved the dog kennel there, settled the dog handlers, and built a wooden church of the Resurrection for them. By the 15th century, the Ascension settlement, located along the Volga, reached these places, and in the 17th century, there were leather workshops in the Debra area. In the early 17th century, there stood a tented wooden urban church of the Resurrection with a chapel of Saint Catherine and a warm church of Cosmas and Damian.

With the increase in the number of residents, the settlement decided to build a stone temple. The greatest contribution to its construction was made by the wealthy merchant Kirill Grigoryevich Isakov from the Gostinaya hundred, who lived nearby. According to legend, among the barrels of paint sent to him from England, he discovered one with gold coins and decided to use them for the church's construction. The church was built by masters from Yaroslavl and Veliky Ustyug. The frescoes of the church were completed soon after its construction, in 1650 and 1652, presumably by the artel of Vasily Zapokrovsky, while the frescoes of the Three Saints chapel, in 1670, are believed to have been done by Guriy Nikitin and his artel.

In the 1740s, the church's windows were enlarged, the gallery openings were bricked up, and the western porch was connected by a covered passage to the Holy Gates.

Originally, there was a bell tower at the church, but in 1801, during the reconstruction of the neighboring warm Znamensky Church, which forms a single complex with the Resurrection Church, the bell tower was dismantled and a new one was built in its place, adjacent to the Znamensky Church.

In 1911 and 1912, the church was partially restored by architect Dmitry Mileev. In 1913, in honor of the 300th anniversary of the House of Romanov, it was visited by Emperor Nicholas II with his daughters and entourage.

During the Soviet era, the church remained active until the 1930s when it was closed and turned into a grain storage facility, and a military warehouse was placed in the basement. In 1946, the church was reopened. According to contemporaries, there were no floors in the church, icons were ripped from the iconostases, and windows were broken. For more than a quarter of a century, starting in 1964, the small church served as the cathedral of the Kostroma diocese. Until 1991, one of the most revered Kostroma relics, the Theodorov Icon of the Mother of God from the destroyed Assumption Cathedral of 1934, was kept here. Restoration work was carried out in the entrance group and Holy Gates in 1967 and 1969.

In 1993, the Znamensky Women's Monastery was established at the Church of the Resurrection on Debra, which also received the partially ruined neighboring Znamensky Church. The church is being restored, and a five-tiered bell tower has been completely rebuilt.