The Smadyn River, flowing into the Dnieper, created a convenient bay for stopping ships, which played an important role in the development of the area as the western port of Smolensk, oriented towards Kyiv. In 1015, Prince Gleb was killed here when his boat was caught by assassins sent by Svyatopolk. In 1019, his remains were transported to Vyshhorod, near Kyiv. Probably soon after the canonization of Boris and Gleb, a monastery was founded at the mouth of the Smadyn in their honor. This likely occurred in the early 12th century when Vladimir Monomakh laid the foundation for the Assumption Cathedral in Smolensk, and it was natural to emphasize the city's connection to the cult of the first Russian saints by establishing a monastery at the site of Gleb's death. The monastery was wooden and likely fortified at the beginning of the reign of Rostislav Mstislavich, so by 1138 it became a base for a political operation: here the exiled prince Svyatoslav Olgovich from Novgorod was captured and imprisoned.

The ideological and political significance of the monastery was highlighted by the laying of a stone church in 1145 by Prince Rostislav Mstislavich. The construction of the cathedral likely continued until about 1150. Notably, the monastery, located away from the city, received a stone church simultaneously with the completion of the Assumption Cathedral. This may be related to the influence of the first Smolensk bishop Manuel, who sought to enhance the ecclesiastical significance of the diocese through the cult of the holy princes and the site of Gleb's death.

The chronicle mentions that in 1197, the Smolensk prince David Rostislavich was buried in the cathedral of the Borisoglebsky Monastery. This suggests that the church was built by Rostislav as a cathedral for the Smolensk princely dynasty. In the 19th century, historian S. P. Pisarev suggested that Smadyn was a fortified princely residence and a large trade and craft settlement, separate from Smolensk.

After the 12th century, there is no direct information about the Borisoglebsky Cathedral, only rare mentions of the monastery's fate. In the late 16th century, the archimandrites Andrey and Theodosius are known. In 1609, Polish troops occupied the monastery, and in 1633 it was handed over to the Uniate Archbishop Lev Krevza. In 1654, the Smadyn area was referred to as 'Zhyhymont's wasteland.' The Church of Boris and Gleb still existed in 1680, but was likely already in ruins. I. I. Orlovsky suggested that the ruins began to be used during Peter I's reign when Smolensk was fortified. In the late 18th century, Governor-General N. V. Repnin allowed the use of stones from the ruins for construction. In 1825, P. P. Svin'in wrote that the ruins were still high. In 1833, Governor N. I. Khmelnitsky ordered the use of bricks and stones from the ruins for road construction, but the work soon stopped. Despite the plundering, the ruins allowed for the determination of the church's layout with its columns and apses.