On September 23, 2017, Metropolitan Alexander of Bryansk and Sevsk conducted the grand consecration of the cathedral in honor of the Annunciation of the Most Holy Theotokos, located on Bezhitskaya Street in the Bezhitsky district of Bryansk, and led the first Divine Liturgy in the newly consecrated cathedral. The Annunciation Cathedral is a subsidiary of the Transfiguration (Spaso-Grobovsky) Church and was built in the Russian style. The project author and builder, General Director of LLC 'Promstroy' Vladimir Konstantinovich Zlotnikov, noted that he aimed to preserve the architectural elements of the Transfiguration Church, albeit in a simplified form. The new cathedral was erected on the site of the three-altar Annunciation Church, which was destroyed in the 20th century. During the foundation laying, builders discovered remnants of the foundation of the previous church, highlighting historical continuity.

The original three-altar stone church was built between 1896 and 1900 on the site of a burned wooden church in the village of Gorodishche, now located on Bezhitskaya Street in Bryansk. The church had two chapels: in honor of St. Nicholas the Wonderworker and in honor of the Protection of the Most Holy Theotokos. In the early 1930s, the church was closed, and the building was used as a hairdresser's, warehouse, printing house, and garage. In April 1971, the church was demolished and dismantled for building materials.

The new history of the Annunciation Cathedral began in 2009 when it was decided to create a memorial chapel on the site of the previous church. Through the efforts of the parish of the Transfiguration Church and with the support of V.K. Zlotnikov, the central part of the chapel was built, but construction was temporarily halted. Metropolitan Alexander of Bryansk and Sevsk, appointed to the Bryansk see, blessed the reconstruction of the chapel into a full-fledged cathedral, as Liturgies could not be conducted in the chapel, and the area was far from other Orthodox churches. The emergence of the cathedral became a long-awaited joy for local Orthodox residents, especially for the elderly and mothers with small children.