The seminary church of St. John the Theologian is located on the second floor of the seminary's educational building in the Znamenskaya Grove, which has belonged to the Znamensky Kursk Monastery since 1722. The building was constructed in 1834-1835 under Bishop Iliodor (Chistyakov) as an archbishop's residence with a chapel. The project was developed by architect G. V. Gavrilov, and the church was consecrated on June 16, 1835.

In 1913, a shelter for the seriously ill and the poor of all classes opened in the archbishop's residence. During World War I, a hospital for wounded Russian soldiers was housed here.

After the October Revolution, the church was closed, and the archbishop's residence became the provincial social welfare department. In the late 1920s, it housed the experimental agricultural station named after the October Revolution, later a fruit and berry technical school. With the formation of Kursk Oblast in 1934, dachas for provincial officials appeared in the Znamenskaya Grove. In the 1950s and 60s, there were several residential apartments in the archbishop's residence, and for some time a children's sanatorium operated there. In 1990, the Znamenskaya Grove became a protected park, and from May 1991 to the summer of 2000, it housed the mother and child sanatorium 'Znamenskaya Grove.'

In October 2001, the Znamenskaya Grove was returned to the Russian Orthodox Church. Kursk diocesan reports stated that by this time, doors, window frames, radiators, pipes, and linoleum had been stolen from the buildings in the grove, and homeless people found shelter in the dacha houses during cold days. Thanks to the efforts of Metropolitan Juvenaly (Tarasov), workers, seminarians, and volunteers, several buildings were repaired, including the former shelter with the church.

On September 1, 2002, services resumed in the church of St. John the Theologian. By this time, 4th and 5th-year seminarians had moved to the grove to live and assist with repairs. Services were conducted by monks from the Znamensky Monastery. By September 1, 2003, the Kursk Theological Seminary had fully relocated to the Znamenskaya Grove, and the church became a seminary church. In 2006, craftsmen from the Orthodox artel in the city of Shchigry installed a new wooden carved iconostasis in the church, and the icons for it were painted by Kursk masters from the icon painting school.

The church houses relics of saints, including St. Blessed Prince Oleg of Bryansk, St. Luke, Archbishop of Crimea, the Optina Elders, St. Innocent, Metropolitan of Moscow, St. Blessed Matrona of Moscow, St. Kuksha of Odessa, St. Eudocia, and Martyrs Daria, Daria and Maria Puzovskaya, St. Alexius of Goloseev, St. Ignatius of Stavropol, St. Joasaph of Belgorod, St. Ambrose of Optina, the Martyrs of Zverinets, St. Elizabeth, the Martyr Varvara, St. Laurence of Chernigov, St. Innocent, Metropolitan of Moscow, St. Athanasius, Bishop of Kovrov, St. Ilya of Murom, and St. Peter, Metropolitan of Kiev (Moscow).