The church is located on the site of the former men's Trinity Monastery, founded during the reign of Boris Godunov. Initially, the Trinity Church was wooden. In 1742, a two-story stone building was constructed, which was then remodeled several times. The lower church became the winter church, while the summer church was placed on the second floor in a more spacious and brighter room.

The Church of the Life-Giving Trinity is one of the oldest churches in Kursk. In 1940, during the Soviet regime, the church was closed, and at the beginning of the Great Patriotic War, the bell tower was removed, and an air defense post was placed in its place. During the German occupation, the church was reopened for services.

The church functioned until 1961. In 1989, the building was renovated and a planetarium was established in it. The diocese returned the first floor in 1992, and the second in 1995. Currently, the church houses the altars of the Holy Trinity, St. Ambrose of Optina, and the holy princes Boris and Gleb in the lower church, as well as the altar of the Holy Spirit and St. Nicholas the Wonderworker in the upper church.

From 2015 to 2018, restoration work was carried out, which included updating the facades, foundation, domes, radial-curvilinear and sloped roofs, as well as canopies.