According to historical data, a monastery existed at this site as early as the 16th century and was destroyed by the Lithuanians. The most common version states that it was founded by the Suzdal Metropolitan Hilarion as a men's monastery, but over time it fell into decline. For a long time, there was no monastery here.

In the 17th century, a wooden parish church of Peter and Paul was built on this site, which was under threat of closure and demolition for about two centuries. By the early 19th century, the church stood in a cemetery. In 1825, the residents of Yuriev-Polsky appealed to the provincial government with a request to demolish the dilapidated Peter and Paul Church. The church was transferred to the Mikhailo-Arkhangelsky Monastery, and in 1830, by decree of the Holy Synod, the church was demolished. For some time, there was a wasteland here, which was handed over to the peasants of the neighboring village of Fedosino. Yuriev merchant Pyotr Borodulin exchanged this land with the peasants and decided to restore the church. On May 16, 1843, the Holy Synod permitted the construction of a stone church. That same year, the construction of a large church in honor of the apostles Peter and Paul began. However, the church remained without a parish for almost twenty years. In 1871, a fire destroyed the women's Vvedensky Monastery, and the nuns were allowed to occupy the Peter and Paul Church, which became the cathedral church of the monastery. By decree of the Holy Synod on January 26, 1874, the monastery was named Petropavlovsky. At the same time, the Uspensky warm church in the neo-Russian style was built.

In the late 19th century, Abbess Klavdiya built a five-tiered bell tower in the neo-Russian style. She also opened a charitable institution and a school for girls, where they taught the Law of God, writing, arithmetic, literacy, sewing, and handicrafts. In the 1920s, the monastery was abolished, and in 1925 all the bells were sold for scrap metal. The Petropavlovsky Cathedral and the Uspensky Church were desecrated, their domes and vaults destroyed, and parts of the walls were damaged.

On May 27, 2010, with the blessing of Archbishop Evlogiy of Suzdal and Vladimir, the revival of the Petropavlovsky Women's Monastery began, which became a dependency of the Nikolsky Women's Monastery. The complex was in poor condition, surrounded by heaps of garbage and trees. Restoration began with the cemetery church of the Ascension, as its walls were better preserved and there was free land for the construction of cells. The first two residents lived in a city apartment and came to the monastery to pray and work, as at that time their own church was still not ready.

On October 15, 2010, the Petropavlovsky Cathedral and bell tower were transferred to the Vladimir Diocese of the Russian Orthodox Church. On October 22, 2015, the Holy Synod decided to open the Petropavlovsky Women's Monastery and appointed Sister Serafima as abbess.

In November 2018, the magazine “Foma” described the life of the monastery: “there are no snow-white walls, instead of bells, a piece of a gas cylinder gathers people for service, there is no crowd of pilgrims under the church, and the school buildings stand mixed with the monastery ones. Three nuns live in the monastery with a dog. The toilet is outside because there is not enough money in the house; the procession consists of one nun walking around the monastery grounds.”

In June 2019, at the initiative of the presidential envoy to the Central Federal District Igor Shchegolev, a working group was created to assist in the revival of the Petropavlovsky Women's Monastery.