The Pokrovsky Monastery was founded in 1708 by Metropolitan Sampson of Astrakhan. Deacon Vasily Kuchukov, a prominent Astrakhan tax farmer, borrowed a thousand rubles from the metropolitan, pledging his garden located between the Kutum River and the Lukovka tributary. Unable to repay the debt, Kuchukov transferred the land to the archbishop, who established a monastery on this site. In the same year, a stone church was built in honor of the Protection of the Holy Virgin with a bell tower. Monks from the archbishop's house settled near the church, and probably at that time a stone fence was erected around the monastery. In 1763, under Bishop Mephodius, two new churches appeared in the monastery: in honor of St. Hilarion the Great in the southern tower and St. Mephodius, Patriarch of Constantinople, in the northeastern tower. In 1790, the monastery became independent. In 1806 and 1808, Astrakhan suffered from a plague epidemic. Many townspeople sought refuge in the Pokrovsky Monastery, believing that the disease would retreat there. A camp formed near the monastery, but the monks, caring for the sick, became infected and died themselves. In 1807, the hospital was moved to the monastery, and the remaining monks were temporarily relocated to other monasteries until September 1808, when they returned to the monastery, which had been cleared of the plague. In 1822, the Voskresensky Boldinsky Monastery, due to its inconvenient location on an eroding bank, was merged with the Pokrovsky Monastery under the name of Pokrov-Boldinsky. In 1867, the Hilarion church was renovated and consecrated in honor of St. Barbara the Great Martyr in memory of the wife of merchant Joakim Repin, who funded the repairs. In 1893, a new abbot's house was built, and in 1903, a new bell tower. In 1900 and 1902, most of the monastery buildings were reconstructed. In 1908, a new church was consecrated on the site of the old one, in honor of St. Mephodius, St. Sampson the Hospitable, and St. Catherine the Great Martyr, the patroness of merchant E. F. Bashkina, who funded its construction. The main shrine of the monastery was the miraculous icon of the Protection of the Holy Virgin. During the epidemic years, many were healed from the plague after praying before it. There are known cases of deliverance from locusts after processions with this icon. The residents of Astrakhan carried the icon to their homes for blessing and prayer.

During World War I, a hospital for 30 patients was opened in the monastery, and 26 refugees were sheltered. With the blessing of Metropolitan Ion of Karpukhin, the restoration of the monastery was supported by the John the Baptist Monastery. On May 14, 2011, the first blue dome and cross were installed on the Catherine Church. On July 6, 2012, Hieromonk Antoniy Azizov served a moleben in the Catherine Church. On May 11, 2013, the first Divine Liturgy after the closure of the monastery was held in the church. In the same year, services were held for the Protection and the feast day of the Catherine Church. On March 14, 2014, the John the Baptist Monastery appealed to the authorities with a request to transfer the buildings of the Pokrov-Boldinsky Monastery, which had previously belonged to the Astrakhan Diocese. At the end of Great Lent in 2015, a new golden dome with a cross was installed on the Catherine Church. On December 7, 2015, an archpastoral liturgy was held in the church under the guidance of Metropolitan Ion of Karpukhin. In the fall of 2016, the building of the St. Catherine Church was transferred to the John the Baptist Monastery, and an oak alley was planted in honor of this event.