Novodevichy Convent in Moscow was founded in 1524 by Grand Prince Vasily III in honor of the return of Smolensk from the control of the Lithuanian principality in 1514, which was an important milestone in the formation of a unified Russian state. The main church of the convent was dedicated to the icon of the Most Holy Theotokos "Odigitria," the main shrine of Smolensk.

From its founding until the 18th century, the convent received significant support from Russian tsars. Among the nuns were relatives of tsars such as Ivan the Terrible, Boris Godunov, and Peter I, as well as representatives of noble families such as Vorotynsky, Kubensky, and Khitrovo. Thanks to generous donations, by the end of the 17th century, the convent became the second richest women's monastery in Russia.

Located at the beginning of the Smolensk road, the convent had strategic significance for the defense of Moscow. Until the mid-17th century, it was part of the capital's defensive system, protecting the southwestern approaches and river crossings. The convent participated in repelling the raids of the Crimean Tatars in 1571 and 1591, and in 1612, a decisive battle for the liberation of Moscow from Polish invaders took place at its walls.

In the 17th century, especially during the reign of Tsarevna Sophia Alexeyevna, the convent experienced a period of prosperity, becoming the summer residence of the ruler. During this time, its architectural ensemble was formed, which has survived to this day. After Sophia's involvement in the struggle for the throne, the convent became her place of exile, where she was tonsured as a nun and died in 1704.

From the early 18th century, the convent lost its status as a court monastery, and after Catherine II's reforms in 1764, it lost its land holdings and was classified as a first-class institution with state support. During the Patriotic War of 1812, the convent was occupied by a French garrison but was saved from destruction by the efforts of the nuns led by the treasurer Sarah Nikolaevna. The gold embroidery workshop founded by Tsarina Irina Godunova continued to operate until the 20th century.

In the 19th century, the awareness of the cultural and historical significance of the convent led to the beginning of restoration work in 1898. After the 1917 revolution, the convent became a museum and was transferred to state ownership, monastic life was interrupted for 72 years.

In 1928, services in the Assumption Church ceased, and in 1929, a "clearing" of the cemetery was conducted, resulting in about 100 of the 2811 gravestones being preserved. After the Great Patriotic War, church life gradually resumed: in 1944, the Orthodox Theological Institute opened, in 1945, services were resumed, and in 1948, celebrations were held for the 500th anniversary of the autocephaly of the Russian Orthodox Church. Since 1964, the Assumption Church has become the cathedral of the Metropolitans of Krutitsy and Kolomna.

By 1980, a large-scale restoration of the convent was completed, and it became a popular tourist attraction. In the fall of 1994, monastic life resumed in the convent, and in 2010, the ensemble of the convent was returned to the Russian Orthodox Church.