In the mid-18th century, in the southwestern part of the Earthen City, on the Kiselyov Hill, a settlement appeared, populated by new residents. It was named Bezrodnaya, as the majority of the population consisted of runaway peasants. They attended the Peter and Paul Church located near the Admiralty. In 1744, the construction of a canal began, which separated the Bezrodnaya settlement from this church. In 1763, when the settlement had about three hundred households, its residents appealed to the Astrakhan bishop Mephodiy with a request to relocate the wooden church of St. John Chrysostom, which was located at the Exaltation of the Cross Church. After receiving permission, the church was moved to the center of Kiselyov Hill that same year, where a parish was established. The wooden church was small and dilapidated, so its clergy, along with the church elder Daniil Ivanovich Plotnikov, appealed to the Spiritual Consistory for permission to raise funds for the construction of a new church. Almost 10 thousand rubles were collected in donations. The church community made an agreement with titular adviser Nikolai Mikhailovich Ladyzhensky for the production of up to one hundred thousand bricks at his factory. The construction of the church took place from 1823 to 1826. The interior finishing was completed by October 1826, and on October 10, the church was consecrated by the Astrakhan Archbishop Pavel Subotovsky. A significant role in the construction was played by benefactor Ivan Petrovich Sharygin. The new stone church was built along with a tall two-tiered bell tower and a stone refectory. Interestingly, the church bells were tuned to a tuning fork.

In modern times, on August 25, 2001, a solemn consecration of the laying of the first stone of the new bell tower took place, completed in 2002. It was built in a classical style, precisely replicating the old forms, and gave the church a harmonious appearance. The church is topped with a powerful helmet-shaped dome on an octagon, set on four walls in the style of 'octagon on square', popular in the central regions of Russia. In the second half of the 19th century, the white facades were remodeled, and reliefs depicting saints appeared on them, reminiscent of the works of Nikolai Nikolaevich Ge, a well-known Russian painter. These reliefs were restored in 1956 and now harmoniously fit into the appearance of the church. Above the entrance to the church is a sculpted figure of St. John Chrysostom, and on the western facade of the bell tower, there are figures of angels in mourning, reflecting the perception of the image and teachings of the Savior by the Russian artistic intelligentsia in the second half of the 19th century. The relief compositions of the Chrysostom Church express the inevitability of suffering, patience, and the strength of asceticism. The exterior of the church today is almost indistinguishable from its pre-revolutionary appearance.