The history of the church began in the 17th century, when in 1663, 31 years after the founding of the city, the residents of Kungur appealed to Tsar Alexei Mikhailovich with a request to allow the establishment of a women's monastery. The tsar granted their request, and the Tikhvin Icon of the Mother of God Monastery appeared in the city.

Initially, a wooden church in honor of John the Theologian was built for the monastery, which was replaced by a stone one in 1758. Five years later, the main chapel of the Tikhvin Icon of the Mother of God was added to the church, consecrated on May 24 (June 4) 1763. Two years prior, the monastery moved to Yekaterinburg, becoming the Novo-Tikhvin Monastery, and the church in Kungur became a parish church. In 1882, the refectory and the old bell tower were dismantled, and a left chapel of the Apostle James and a new 70-meter bell tower were added, designed by architect A. B. Turchevich. The work was financed by merchant Dubinin, and significant donations were made by Kungur merchant Y. S. Gubkin. The Tikhvin Icon of the Mother of God became the main shrine of the church.

In 1935, the church was closed. It remained closed for several years, but in 1950, a children's cinema opened in its building, which operated for more than half a century and was recognized as the best children's cinema in the Perm region under director Tamara Stafeyeva.

In the 2000s, restoration work began on the church: a major renovation of the bell tower and roof was carried out, and a golden spire was installed. In 2002, the cinema moved to a branch of school No. 18, the church underwent repairs, and in 2004, 11 bells made in Kamensk-Uralsky were installed, which rang for the first time in Kungur on March 14, 2004. A new iconostasis was consecrated in the central chapel of the Tikhvin Church on July 9, 2008.

In 2008, the church celebrated its 250th anniversary.