The legend of the monastery's foundation is presented in the Life of Abraham of Rostov. According to tradition, there once stood a stone idol of Veles at this site, which the local inhabitants worshipped. The idol was destroyed thanks to the apostle John the Theologian, who appeared here after the hermit Abraham prayed and gave him a staff with which the idol was shattered. On the site of the destroyed pagan shrine, the hermit built a church and founded the monastery. However, in historical science, the time and circumstances of the monastery's foundation remain disputed. Evgeny Golubinsky and Arseny Kadlubovsky do not recognize Abraham as the founder of the monastery, first mentioned in the Laurentian Chronicle in 1261, and consider him a church figure of the 14th century. Most scholars believe that the original version of the life was written in the 15th century.

The staff of Abraham remained in the monastery for a long time. Before the campaign against Kazan, Tsar Ivan the Terrible visited the monastery and took the staff with him. After the capture of Kazan in 1553-1555, the tsar built a cathedral in the monastery in honor of the Epiphany of the Lord. This is one of the first multi-altar churches of the mid-16th century, where the program of dedications is expressed in the arrangement of side churches. During the Time of Troubles, the monastery was plundered by the Poles. In the mid-17th century, under Archimandrite Ion, stone churches of the Introduction and the gate church of St. Nicholas were erected. In 1914, the Euphrosinia Polotsky Women's Monastery and the Vitebsk Diocesan School were temporarily transferred to the monastery, and the inhabitants moved to the Spaso-Yakovlevsky Monastery. After the canonization of Dmitry of Rostov in the mid-18th century, the Spaso-Yakovlevsky Monastery became more prominent, while the Abrahamiev Monastery faded into the background, although it continued to be visited by members of the royal family, as well as John of Kronstadt and Patriarch Tikhon.

In 1923, believers from the surrounding villages organized a religious community in the monastery, the first abbot of which was Archimandrite Neophyte Korobov. On March 3, 1926, the buildings of the monastery were transferred to the Rostov Museum of Antiquities, but the community existed until July 16, 1929, when it was liquidated by the decree of the Presidium of the All-Russian Central Executive Committee. After the closure, the clergy supporting the community began to serve in the Assumption Cathedral of Rostov. In 1930, the destruction of the monastery walls began. The Epiphany Cathedral was turned into a grain warehouse, the St. Nicholas Church into a military unit and housing, and the Introduction Church into a kindergarten, then a sanatorium and a sobering-up station. By the end of the 20th century, all buildings were in urgent need of repair, especially the Epiphany Cathedral, which was in an emergency state.

In the 1990s, the monastery was revived. In 1993, a dependency of the Church of the Not-Made-By-Hands Image of the Savior of the Moscow Andronikov Monastery was established here, which was transformed into a Patriarchal dependency in 1994. The duties of the abbot were performed by Priest Vyacheslav Savinykh. In 2004, with the blessing of the Holy Synod of the Russian Orthodox Church, the dependency became the Abrahamiev Epiphany Women's Monastery of the Yaroslavl Diocese. The Epiphany Cathedral remains in an emergency state. Restoration works have drawn criticism from urban preservationists and heritage protection authorities, as the new elements do not correspond to the historical appearance. In 2015, during the restoration work, the vaults of the porch collapsed. In March 2016, the Abrahamiev Monastery was mentioned in a series of broadcasts "Assault on Heritage," dedicated to the unsatisfactory condition of historical and architectural monuments in Russia.