Next to the Demidov estate, on an island, stands the oldest church of the Descent of the Holy Spirit upon the Apostles, known as the Old Church. In the Southern Urals, it is the second oldest stone church, surpassed only by the Uysky Trinity Cathedral in Troitsk. It is one of the few churches in the Baroque style that has hardly undergone reconstruction and was built alongside Kyshtym, witnessing its entire history.

According to legend, in 1755, after surveying the surroundings and beginning the construction of a factory, Nikita Nikitich Demidov dined on the island and proclaimed: "Let the people know where Nikita dines! Build a church here!" This decision still astonishes researchers. G.H. Samigulov notes that the church was not built in the center of the settlement or on a hill, but on an island in the middle of a pond. This is an unconventional decision, as churches or mosques are usually not separated from settlements by water. Nevertheless, construction began immediately. Stone was delivered from the Kyshtym and Sugomak mines, where it had accumulated sufficiently after stripping operations. An unusual architectural project was chosen.

The church was built on a grand scale: two stories, made of brick and stone. Materials were lifted manually or with the help of simple winches. For a provincial church, it turned out to be ornate and majestic. The upper floor was dedicated to the Descent of the Holy Spirit, while the lower one was dedicated to the Beheading of John the Baptist. The upper floor was not heated, and services were held there in summer, while the lower one operated year-round.

Construction took five years, financed by factory owners and local residents. In 1764, the work was completed, and the church was painted by the God-loving Bogatyrevs. Local historian B. Meshcheryakov indicates that the church was consecrated by the priest of Yekaterinburg, Fyodor Kochnev, on February 7, 1765. The first test the church faced was during the Pugachev Rebellion. In January 1774, rebels broke through the wooden walls of the factory. It is said that the church elder, Yefim Norkin, rang the alarm bell and was thrown from the bell tower. The Pugachevites camped around the church, let horses inside, lit fires, removed the vestments from the icons, and pierced them with spears.

Father Alexiy Gornykh reported that the rebels broke the doors and windows, killed the sacristan, and took all valuables from both churches. After their retreat, it took a year to restore the church. On February 1, 1775, it was consecrated again by priest Vlasiy Korovitsky. The second trial came during the Soviet 1920s-30s when the church was closed and looted but not blown up. The building housed warehouses, a printing house, a cinema, and a city museum. The church deteriorated, the domes rusted, plaster fell off, and the floors rotted.

In 2000, the restoration of the church was taken up by parishioners led by Father Nikolai Gashkov. First, they repaired the first "warm" floor, where services began, then work continued on the second floor and the 44-meter bell tower, which offers a view of Kyshtym. In December 2002, Metropolitan Ioann consecrated the church again, for the third time in its history. In August 2015, the scaffolding was removed, and in November, for the first time in many decades, the sound of the bells rang out over the factory pond.