The monastery was founded in the 1680s by schemamonk Zosima, who came from the Trinity-Sergius Monastery and gathered a small community around him. Over time, pilgrims began to flock here, including Peter I's sister, Natalia Alexeyevna. However, after the elder's death, most of the monks left the monastery, and it fell into disrepair. Nevertheless, local residents continued to venerate the righteous man's grave as a shrine. According to legend, the future Empress Elizabeth Petrovna visited here, having lived for a long time in the neighboring city of Alexandrov.

In the late 1890s, the monastery was restored through the efforts of Archimandrite Pavel Glebov from the Trinity-Sergius Lavra and Hieromonk Herman Gomzin, who became the builder of the monastery in 1896 and died on January 30, 1923. The monastery became one of the centers of eldership.

From 1897 to 1923, the monastery was led by schemamonk Herman. During this period, all the surviving stone buildings made of red brick in the Russian style were constructed. In 1900, the main church in honor of the Smolensk Icon of the Mother of God was consecrated.

From 1898 until the monastery's closure in 1923, Elder Alexiy Solovyov lived here, residing in the "elderly" building by the Holy Gates, which was built with the funds of Grand Duchess Elizabeth Fyodorovna.

In 1917, Makariy Nevsky temporarily lived in the monastery. The monastery was frequently visited by members of the Moscow religious-philosophical circle led by Mikhail Novoselov, who sought to attract his friends here, including Nikolai Berdyaev and Sergey Bulgakov. Pavel Florensky also regularly visited Zosimova Monastery.

In May 1923, the monastery, functioning as an artel, was finally closed.

It was revived in April 1992. In July 1994, the founder of the monastery, schemamonk Zosima, was canonized for church-wide veneration, as well as the Venerable Herman Gomzin at the diocesan level. In 2000, Venerable Alexiy Solovyov was canonized for church-wide glorification.