In 1568, Churkin Island along with the adjacent uchug was transferred to the Astrakhan Trinity Monastery. According to the monastery's tradition, the first church at this site was built by the founder of the monastery, the venerable igumen Kirill, and consecrated in honor of Saint Nicholas the Wonderworker. Venerable Kirill donated an icon of Saint Nicholas to the church, which later became famous for miracles and healings. In the mid-17th century, another shrine appeared here, the miraculous Smolensk icon of the Mother of God. According to tradition, in 1669, when Stepan Razin's bandits were robbing the lower Volga, they attempted to burn the icon, but the fire turned against them, and the icon miraculously ended up on the monastery's uchug. The monks honorably placed it in the Church of Saint Nicholas the Wonderworker, and many miracles occurred from it.

In the 17th century, Churkin's uchug passed to the Astrakhan Spaso-Preobrazhensky Monastery. The monks lived here by the church on the banks of the Churka River. In the 1670s, a new inhabitant appeared here, the executioner Laryka, who, realizing his sins, retreated here and dug himself a cave. He remained in the people's memory as Churka. After his death, other ascetics began to dig caves in the hill, and now, according to local residents, there are many passages inside the hill. In the early 18th century, the Church of Nicholas was moved to the 'High Mountain,' as Churkin Hill was called. In 1762, Churkin Monastery became an independent monastery and experienced a flourishing period under Bishop Mephodiy. A stone church and a fence were built, and the monastery had a rich garden and a herd of horses.

The monastery thrived until 1806, when its fishing waters were taken by the treasury, and the monastery fell into decline. A new revival is associated with Archimandrite Eugene, who became the abbot in 1840. Under him, Churkin Monastery gained significance comparable to Optina Monastery. His successor, Archimandrite Paisiy, built the Assumption Cathedral and restored the monastery's waters. Paisiy, a student of Glinskaya Monastery, began to align the monastery's rules with its strict regulations. His work was continued by Archimandrite Makariy Zhirov, who brought monks from Glinskaya Monastery. In 1910, the John the Forerunner Skete was founded, with Hieromonk Dosifei Kuzmin as its abbot.

In the early 20th century, the monastery flourished, with a brick factory, workshops, gardens, and livestock. However, in 1919, the monastery was closed, and its economy fell into decline. In 1930, the bell tower and cathedral were demolished, and the bricks were used for construction in the settlement named after Volodarsky. Later, the territory of the monastery housed an orphanage, a sanatorium, and hospitals. The last one here was a psychiatric hospital, closed in the early 1990s.