According to the scribal books of 1630, there were two village churches in the Yakhrenka parish at that time. In 1760, the construction of a two-story stone church began with funds from P. Kokovin. The lower warm church was consecrated in 1775 in honor of Nicholas the Wonderworker. The work was commissioned by merchant M. I. Murogin with the support of the parish community under the guidance of A. Shekhirov. The main altar of the upper church was consecrated in 1781.

The church was built in the best traditions of the Veliky Ustyug baroque of the mid-18th century. The volumetric-spatial scheme of the "refectory" type acquired a centralized form, elongated along the west-east axis. The central part became a square with three levels of openings, topped with a large light octagon and a small blind one serving as the neck of a small dome. The transition to the octagon was supported by half-domes placed along the axes of the facades. From the east, the church masses increased with a stepped composition of altar apses. From the west, a shortened refectory, equal in length to the upper apse, was complemented by a wooden porch with stairs to the second floor. The capitals made of colored majolica, unique works of Ustyug masters, adorned the pilasters of the church.

In the first half of the 19th century, a free-standing bell tower was built next to the Epiphany Church, strictly along its longitudinal axis. The two-tier square base with semicircles of the pediments supports an octagonal pillar with ringing arches at the top. The bell tower is crowned with a slender spire with a thickening at the bottom in the form of a "kubyshka," set on an elongated pedestal. The architect managed to preserve the dominant role of the church and the artistic unity of the ensemble.

During the construction of the bell tower, repairs were made to the church, resulting in the facades receiving a new finish in the classical style. The brick profiling of the details was changed, new decorative elements, alabaster cherubs, stucco garlands, and balusters were added. The original coloring was replaced with ochre and white details. In those years, master Tomilov painted the interior of the upper church. The altar compositions "The Last Supper" and "Descent of the Holy Spirit" created by Y. F. Gribanov have been preserved.

In 1872, the church building was extended, connecting the refectory with the bell tower. A two-flight white stone staircase leading to the summer church appeared on the first floor. Two adjacent rooms were designated for a storeroom and a sacristy. The lower tier of the bell tower was surrounded by tents: the southern one was allocated for a burial place, and the northern one for a watchman's room. The entrances to the church were adorned with covered porches. A third altar was arranged in the lower church, consecrated in 1874 in honor of Zosima and Savvatiy, marked by a small drum with a dome on the northern slope of the roof.

The next major repair and painting in the upper church took place in 1898 and 1902. The painting work by master I. V. Kalinovsky was completed with the reconsecration of the church on September 8, 1902. External repairs were carried out in 1904: the roof was covered and painted, the domes and crests were gilded, and the facades were updated. The work was carried out by A. Samoilov and Y. S. Vereshchagin. After a fire on May 12, 1914, the carved iconostasis and wall paintings in the upper church were damaged. Restoration work was carried out by N. Z. Kapchenko from August to October 1914.

In 1983, the building of the Epiphany Church was declared a monument of local significance and placed under protection. The study and restoration project was carried out by the cooperative "Restorer" in 1990-1991.