From 1524 to 1526, a stone church of the Annunciation was built on the site of an old wooden church to the west of the Cathedral of Boris and Gleb. This is one of the few structures whose authorship is documented to the talented Rostov architect Grigory Borisov.

The church has a cubic shape and is topped with a four-pitched roof with an onion-shaped dome set on a thin drum, decorated with an arcature-columned belt. The building's facades are divided into three parts by light pilasters. Initially, the church had narrow window openings, similar to those preserved on the end wall of the refectory. The interior space of the temple, which has no columns, is covered with a ribbed vault. It is suggested that due to this vault design, the roof was originally not four-pitched but three-bladed, like in the Ascension Church in Rostov, also built in the 16th century. Under the modern roof, the lower part of the ancient drum made of profiled brick, which once rose above the roof, has been preserved.

Documents have not preserved information about the painting of the Annunciation Church, and now its walls are white. However, in the 1990s, fragments of paintings dating back to the 17th or even 16th century were found during restoration. Among them is part of the figure of the Mother of God in a pose characteristic of the composition "Annunciation," and a fragment of an inscription confirming the depiction of this scene on the wall. The appearance of the church changed significantly after the reconstruction at the end of the 17th century: new windows were installed, facades were altered, the drum was raised, and the shape of the dome, which was originally helmet-shaped, was changed. These changes are confirmed by monastery documents mentioning the consecration of the church, which took place both during its construction and after major reconstructions. The Annunciation Church was first consecrated on October 4, 1526, and for the last time in 1882 after significant repairs, when remnants of ancient frescoes were possibly removed. The church was also consecrated on November 17, 1696, likely after a major reconstruction.

The temple stands on a high podklet, which was used as a "brotherly pantry" in the 17th-18th centuries. At the current entrance to the sub-church, there was likely a wide window before. The southern facade of the building changed after the appearance of wide windows, the central part of the pilasters was trimmed and framed with decorative moldings with fine brick carvings, characteristic of the altar added at the end of the 17th century. The octagonal window in the middle of the southern wall is typical of "Naryshkin" architecture, widespread in Russia from 1690 to 1710, indicating the time of the building's reconstruction. To the west, the refectory adjoins the church, a square-plan single-column structure with cross vaults.

Along with the Annunciation Church and the refectory, there is one of the oldest civil buildings of the Borisoglebsky Monastery, the abbot's quarters, built on a high podklet due to the terrain. From 2010 to 2015, restoration of the Annunciation Church and the new abbot's quarters was carried out. The church's brick wall and vault masonry, plastering, wooden staircase, as well as volumetric and cut carvings of columns, railings, and balusters were restored. In the western wing, the brick masonry was restored, the metal railing of the staircase was restored, ceramic tiles were made and installed, dolomite floors, window and door openings, as well as metal grilles and the framework of the porch fence were restored. In the new abbot's quarters, ceiling beams were reinforced, brick wall and vault masonry, plastering, staircase and its metal railing, as well as floors were restored.