The church is first mentioned in the 18th century, when in 1773 construction of a new stone church began on the site of the cemetery chapel. A cold church in honor of John the Baptist was built, consecrated on May 29 (June 9) 1787, and a warm chapel in honor of St. Nicholas the Wonderworker, consecrated on December 2 (13) 1792. The church was small, measuring 9.5 fathoms in length and 3.5 fathoms in width, with the cold church occupying most of the space. The bell tower was small and low, and the church did not possess rich furnishings.

The new church was assigned to the Annunciation Cathedral, and until 1835, services were conducted by the cathedral clergy, as well as priests from other churches in Kungur. Due to the cramped conditions, there was not enough space for worshippers, and in 1867, plans were made for its reconstruction with the addition of two chapels. However, due to the church's poverty and small congregation, it was decided to transfer the church to the Kungur Women's Monastery, and the congregation was assigned to the Tikhvin Church, which led to the suspension of the reconstruction. Nevertheless, in 1872, the congregation of the John the Baptist Church was preserved.

On May 9 (21), 1886, a new chapel in honor of the icon of the Mother of God and martyr Christopher was laid on the eastern side of the church. In 1889, with donations from merchant A. P. Chuloshnikov, the church was adorned with paintings. In 1892, a large-scale reconstruction of the church began under the guidance of Perm architect A. B. Turchevich.

On April 9 (April 27), 1894, the last Liturgy was held in the John the Baptist chapel, and on May 22 (June 3), 1894, new chapels were laid in place of the demolished chapel.

After the October Revolution of 1917, the life of the church gradually faded, and on January 9, 1931, it was closed. Its premises were used for blacksmithing and welding sections and belonged for a long time to a nearby colony. The interior was completely remodeled, and the artistic painting was lost.

On August 1, 1990, the church building was returned to the believers, and in the following years, it was gradually repaired. In 1996, Patriarch Alexy II visited the church, and in the same year, 7 new bells were cast for the church, and on September 17, 1997, a tent was installed on the bell tower.

The church is active and recognized as a cultural heritage site of regional significance.