The history of the Annunciation (Resurrection) Church on Moscow Street is closely linked to the Annunciation and Resurrection Cathedrals, which existed in Kursk on Red Square until almost the end of the 18th century. After their closure due to dilapidation, a new two-story Annunciation Church, built between 1801 and 1809, became the successor of these ancient temples and the guardian of their treasures. Among them are: a silver cross with relics of saints, gifted by Tsar Alexei Mikhailovich to the Kursk Resurrection Cathedral; the ancient icon of the Mother of God "Life-Giving Spring"; the old image of the Resurrection of Christ; icons from the Annunciation and Resurrection Cathedrals used in the iconostases of the lower and upper floors; bells from both cathedrals and other relics.

The church is a two-story brick building with one dome, designed in the classical style. The composition is based on the type of centralized church "trikonkh," where three semicircular apses adjoin the square under the dome from the north, east, and south. This is a rather rare phenomenon for Russia, but common in the church architecture of Armenia and Georgia since the 6th century. The central part is designed in the style of an octagon on a square, with a central nave adjoining from the west under a four-pitched roof topped with a two-tiered bell tower. The lower church had two altars: the Annunciation and St. Paraskeva Friday (consecrated in 1801), and in the upper church, the Dormition of the Mother of God (consecrated in 1802).

In 1898, a parish school for boys was opened at the church, which operated until 1906. In the same year, a new two-story brick parish school for girls was built with funds from engineer Konopatov. On November 20, 1934, the church was closed, and the building suffered destruction during the Great Patriotic War and significant renovations in the 1930s and 1940s.

Today, both buildings, connected by a modern passage, house a music college. The eastern apse and the central dome of the Annunciation Church have survived, surrounded by modern extensions of the college.