It is not clear when the monastery was established. Its name is probably derived from the Russian word for "living together", possibly because nuns were allowed into the cloister prior to 1504.
Most of the monastery buildings were erected at the turn of the 18th and 19th centuries, when the monastery was being renovated as a centre of Russian staretsdom. In 1821, a hermitage for startsy was established 400 metres (1,300 ft) away from the monastery. The startsy attracted crowds of devout Christians to Kozelsk. Among others, Optina Pustyn was visited by Fyodor Dostoevsky, Vasily Zhukovsky, Nikolai Gogol, Ivan Turgenev, and Vasily Rozanov. Leo Tolstoy also visited the monastery, although he didn't approve of the staretsdom.
The cloister boasted a rich library, collected with help from the Slavophile Kireyevsky brothers, both buried within the monastery walls. The philosopher Konstantin Leontyev lived at the monastery for four years and took the tonsure here. The local starets Saint Amvrosy is said to have been a prototype of Father Zosima in Dostoyevsky's novel The Brothers Karamazov.
After the Russian Revolution, the last of the startsy were forcibly deported from the monastery, which was declared a gulag. The last hegumen was executed in Tula in 1938. Later, some of the structures were demolished, while the cathedral was designated a literary museum.
In 1987 with the beginning of Perestroika, Optina Pustyn was one of the first abbeys to be returned to the Russian Orthodox Church. In the 1990s its most notable startsy were glorified as saints. They are commemorated together on October 10 (October 23 on the Gregorian Calendar).