It is believed that the monastery was founded in the late 12th or early 13th century by Greek missionary monks who brought with them a miraculous icon of the Apostle John, painted in the 6th century in Byzantium by an orphan boy. This icon became the main shrine of the monastery. V. V. Zverinsky reports that the monastery already existed in 1237, and by that time it housed the miraculous image of John the Theologian, gifted by the Ryazan prince and, according to legend, protected the monastery from being plundered by Batu.

In the 16th and the first half of the 17th century, the monastery was repeatedly ravaged by the Crimean Tatars, but was restored each time. Known devastations occurred in 1534 and 1572. It is likely that the Poshchupovo cave, located nearby, is part of the monastery. Originally, the monastery was located further south, but in the 16th century it was moved to its current location. Until the mid-17th century, all buildings were wooden. In 1764, almost all the lands of the monastery were confiscated, and it was classified as a third-class monastery, leading to its decline by the mid-19th century.

The revival of the monastery is associated with David Ivanovich Kludov, a first-guild merchant. In 1860, he purchased a country estate near the monastery. The St. John the Theologian Cathedral was completely reconstructed, and a new iconostasis was installed, for which the icons were painted by the Ryazan artist Nikolai Vasilyevich Shumov. On March 22, 1865, hieromonk Vitaly Vinogradov became the abbot. The monastery was transformed into a communal one, the cathedrals were restored, the fence was repaired, and a new bell tower was built according to the design of I. S. Tsekhanovsky. Hieromonk Vitaly, who later became an archimandrite, managed the monastery for half a century and died in 1915 at nearly 100 years of age. Under him, the number of brethren increased to more than 100 people. By 1892, a school for peasant children with 50 places was opened at the monastery.

In 1930, the monks led by Archimandrite Zosima Musatov were arrested and exiled to Kazakhstan. The monastery was closed, and soon the ancient icon of the Apostle John the Theologian disappeared, its whereabouts unknown. Initially, a children's colony was placed on the monastery's territory, then warehouses of the Ministry of Internal Affairs. In 1988, the monastery was returned to the Russian Orthodox Church, and its restoration was undertaken by Archimandrite Abel Makedonov.

In 2004, the management of the monastery was entrusted to Bishop Joseph, vicar of the Ryazan diocese, who became the first hierarch abbot in the history of the monastery. In the summer of 2006, he was appointed to manage the Ivanovo-Voznesensk diocese.

Currently, the abbot of the Holy St. John the Theologian Monastery is Metropolitan Mark Golovkov, who manages the Ryazan diocese.