At the site of the modern Znamensky Monastery, there was a city fortress of Kursk in the early 17th century, built in 1596 on the site of an ancient pre-Mongolian settlement on a high cape at the confluence of the Tuskar and Kur rivers. In 1612, Kursk was captured and devastated by the Polish-Lithuanian army under the command of Hetman Zholkevsky, numbering about seventy thousand men. The only place that the enemies could not take was the city fortress, defended by Voivode Yuri Ignatievich Tatischev. The defenders of the fortress, suffering from a lack of water and gunpowder, vowed to build a monastery in honor of the Kursk Root Icon of the Mother of God "Znamienie" if they succeeded in defending the city.

A month after the unsuccessful siege, the enemies retreated, and the Kursk residents began to fulfill their vow: first, a wooden church was built in honor of the Nativity of the Most Holy Theotokos. In 1613, Tsar Mikhail Fyodorovich Romanov allowed the establishment of a monastery next to the new church, and its construction was completed by 1615. In 1631, the monastery suffered from a fire caused by a lightning strike.

By the decree of Tsar Alexei Mikhailovich in 1649, a stone cathedral in honor of the Icon of the Mother of God "Znamienie" was laid on the site of the wooden church, which was built by 1680 with funds from the royal treasury and private donations. After that, the monastery became known as the Nativity of the Mother of God Znamensky. At the same time, other churches and buildings were constructed with donations from the Romanov princes, as well as a stone wall with towers.

According to the manifesto of Catherine II on the secularization of monastery lands from 1764, the Znamensky Monastery was classified as second class and remained part of the Belgorod and Oboyansk diocese. In 1816, the construction of the large Znamensky Cathedral began, which became a monument to the victory in the Patriotic War of 1812. In 1854, the monastery was granted first-class status.

The monastery was closed by the Bolsheviks in 1924, and a local history museum was established on its territory. The Znamensky Cathedral was used by believers, while the brotherhood building served as a dormitory. In 1932, the Znamensky parish was liquidated, and a cinema "Oktyabr" was arranged in the cathedral, which opened in 1937.

The monastery was reopened in 1992, and the reconstruction of the Znamensky Cathedral began. In 2000, Metropolitan Juvenaly of Kursk and Rylsk consecrated the main altar of the cathedral. In 1997, a decision was made to transfer the Resurrection Church to the Russian Orthodox Church, which effectively took place in 2003. In 2006, a dome was installed on the church.

The building of the House of the Hierarch now houses the Kursk Regional Local History Museum. On January 15, 2013, Schema-Metropolitan Juvenaly was buried in the grounds of the Znamensky Monastery after the Divine Liturgy.