In the historical center of Kharkiv, where Pushkinska Street meets an ancient park, stands the Church of the Beheading of St. John the Baptist, built in the Russian-Byzantine style. The architect of the church was Andrei Andreevich Ton, an academician of architecture. In 1857, the church was consecrated by Archbishop Innocent Borisov of Kharkiv and Akhtyrka. The first rector was Priest Ioann Chudnovsky, who died on February 18, 1859, and was buried by the northern wall of the church.

In the Kharkiv calendar of 1878, published by the Kharkiv Statistical Committee, the cemetery church of the Beheading of St. John the Baptist is mentioned in the section about churches in the city without parishes. The rector was Priest Onikevich Nikandr Ivanovich, and his assistant was Priest Volobuev Georgiy Ivanovich. Father Nikandr also served as an inspector and law teacher at the Kharkiv Diocesan Women's School located nearby and held a degree of Candidate of Theology from the Kyiv Theological Academy. Father Georgiy was also an assistant law teacher.

From 1882 to 1884, the well-known Kharkiv theologian, writer, and historian Protopriest Timofey Ivanovich Butkevich served in the church, making a significant contribution to the spiritual life of the city. In 1903, Protopriest Ioann Khristoforovich Picheta, originally from Serbia, became the rector and actively developed the spiritual schools of the Orthodox Church.

In the 1920s, the church was seized by Renovationists and closed, but it was not destroyed. Its interior decoration was destroyed, and church utensils and icons were looted. The church may have survived due to its location deep within the cemetery. In 1941, German troops, aware of an ammunition depot in the church, shelled it, but the building suffered little damage. In 1943, after the liberation of Kharkiv, services resumed, and the church began to be restored.

In 1970, Father Yaroslav Bovtyuk became the second priest of the church, who led the parish after a year and a half. In 1987, a new church in honor of St. Job of Pochaev was built on the church grounds. Protopriest Yaroslav Bovtyuk dedicated over 50 years to pastoral service, more than 40 of which were to the John the Baptist Church. He was awarded numerous church orders for his many years of labor.