According to the first written records, by 1710 the Epiphany Church was wooden and had two chapels. It stood for about 30 years but burned down in 1729. By 1731, the church was restored. The Epiphany Church was located next to the churches of Flora and Lavra and the Holy Martyr Blasius.

The construction of the stone Church of the Epiphany, replacing the wooden one, began on May 15, 1805, and lasted a year. It was a two-story building with a dome and five heads on wooden faceted drums, standing 32 meters tall. The main chapel was consecrated in the name of the Epiphany of the Lord, and the chapel on the second floor was in the name of the Holy Life-Giving Trinity. To the west, a refectory adjoined the church, heated in winter by stoves, with two chapels: to the left of the entrance in honor of St. Nicholas the Wonderworker, and to the right, St. George the Great Martyr.

The church suffered greatly during a storm in 1841, after which it was repaired and the altars reconsecrated. The bell tower, built in 1834, soon began to deteriorate. In 1895, Vologda provincial architect Remer decided to dismantle it to the ground. On October 12, 1897, the construction of a new bell tower began, completed in 1904. Its height was 52.5 meters.

From 1904 to 1914, work was carried out to expand and arrange the two-light church: the vaults were relaid, the height of the walls of the refectory and main church was increased, and the second floor of the summer church was abolished to increase the volume of the church and create a second light in the form of round windows under the cross vaults. Thus, the church acquired its modern appearance.

During the Soviet era, the church fell into disrepair and destruction. In 1922, a campaign to confiscate church valuables took place in Pezhma, and many priests were repressed. In 1937, the church was closed by the decision of the presidium. The bells and the cross from the bell tower were thrown down, and the property was removed. The church building was used as a grain storage and warehouse, and the cemetery area was turned into a parking lot. Two two-story houses were built on the north side, and on the south side, after a fire that destroyed the Flora-Lavra church, a road was laid to the bridge over the Pezhma River.

In the 1990s, a restoration project for the Epiphany Church was developed, the interior was cleaned, and mountains of garbage, metal, and years of dirt were removed. Dozens of meetings, consultations, gatherings, and trips took place, but funds for complete restoration were lacking. Major reconstruction began only in June 2009, and the first liturgy was held just a month later.