The main premises of the monastery, carved into the caves, are located on the western cliff of the Monastery Rock, on the plateau of which the ruins of the medieval fortress Kalamita, founded in the 6th century, have been preserved. In the 14th-15th centuries, the fortress became part of the Orthodox principality of Theodoro and protected its port, but in 1475 it was captured by the Turks. Historians date the foundation of the monastery differently: from the 8th-9th to the 14th-15th centuries.

According to legend, the monastery arose in connection with the veneration of Clement, the Roman bishop, who was exiled by Emperor Trajan for preaching Christianity in the quarries near Chersonesus and was killed here in 101 AD. The relics of St. Clement, discovered a year after his death, were initially kept in an underwater grotto near Chersonesus, accessible once a year when the sea receded. Later, they were transferred to an island where, according to legend, angels built a church. Around 861, the relics were found by Saints Cyril and Methodius and transferred to the Chersonesus temple, where miracles occurred through the prayers of the saint.

Near the monastery was a spring opened by St. Clement to alleviate the plight of convicts. In the 1970s, the spring dried up, and its water flooded a quarry for Inkermań stone on the other side of the cliff.

After the Turks captured the fortress of Kalamita in 1475, the monastery fell into decline. The fortress was renamed Inkermań, which gave its name to the city that belonged to Russia since 1783.

In 1850, the monastery was revived and received its modern name in honor of the city and St. Clement. In 1867, a cave temple of St. Martin the Confessor was redesigned and opened. In 1895, a temple in honor of the Great Martyr Panteleimon was built in memory of the salvation of the royal family, and in 1905, the church of St. Nicholas of Myra was built in memory of the Crimean War.

Since 1924, the temples of the monastery began to close. In 1927, an earthquake damaged the Annunciation and Nicholas churches, and they were dismantled. In 1928, the temple of the icon "Joy of All Who Sorrow" was closed. In 1931, services in the cave temples ceased, the monastery was finally closed, and its property was transferred to the Sevastopol Museum Association. After the closure, the abbot Benedict, Father Prokopiy, and two elders remained living in the monastery.

During the Great Patriotic War, the headquarters of the 25th Chapayev Division of the Primorsky Army was located in the caves of the monastery. In June 1942, soldiers of this division held back the advance of German troops on Sevastopol at the Inkermań heights.

Since 1991, the gradual revival of the monastery began under the guidance of Archimandrite Augustine, the brotherhood, and laypeople. The temples and cell buildings were restored, and a part of the head of St. Clement was brought from Kyiv, which was installed in the side nave of the St. Clement's Church.

On January 26, 2019, weekly services resumed in the cave temple complex, in the church of Clement of Rome.