The temple was built on the site of a white-stone cathedral from the 14th century. The beginning of its construction in 1648 marked the start of stone works in the Annunciation Monastery when Velyamin Cheretkin received a royal decree allowing the duty-free transportation of bricks from Balakhna. Iron for the fastenings came from the patriarchal storages of the Moscow Kremlin. Chronicles indicate that construction was completed in 1649.

The architecture of the temple is unique and possesses its own characteristic artistic and structural features. Although it was built as a six-pillar structure, the vaults and domes are supported by four pylons. The western pair of columns is absent, and the resulting space is covered by a closed vault with arches. The eastern wall, like in Yaroslavl churches, stands on altar vaults. The domes have different shapes: the central one is onion-shaped, while the four smaller side domes are helmet-shaped. The zakomaras are made with a three-centered outline, reminiscent of the barrel roofs of ancient Russian buildings. Beneath the building is a sub-church used as a storage room, with two entrances where carts could enter via a ramp from the northern side.

Initially, the central dome of the cathedral was covered with glazed tiles, while the side domes were covered with white iron. The open porches inside were decorated with frescoes, and the western and northern entrances had barrel roofs. After several fires in the 18th century, architect Y. A. Ananyin carried out repairs in 1780 and 1785, replacing the zakomara roof with a four-pitched one.

The cathedral's iconostasis was adorned with numerous ancient icons, inlaid with precious stones and pearls, including the Mother of God with the attending figures, the image of Metropolitan Alexius in the life of the 14th century, and others. In 1820, icon painter P.P. Korin from Palekh created new images on the old twelve boards.

In 1825 and 1827, architect I. E. Efimov conducted repairs on the cathedral. In 1870 and 1872, academician L. V. Dal carried out restoration, returning the temple to its original forms.

From 2004 to 2007, construction and restoration work was carried out in the temple, and the heating system was replaced, allowing services to be held in winter. The walls were also whitewashed inside and outside, the entrance was updated, and the gallery was reconstructed.