The monastery was founded by Saint Galaktion of Vologda in the early 17th century and was originally called Galaktion Desert. Until 1654, all its buildings were wooden. In that year, thanks to donations from Tsar Alexei Mikhailovich, a stone cathedral was built in honor of the Descent of the Holy Spirit, and the monastery was renamed Holy Spirit.

In 1775, by decree of the Holy Synod, the monastery was renamed Spaso-Kamenniy, in honor of a burned and abolished monastery of the same name, whose brethren were transferred to the Vologda Holy Spirit Monastery.

Around 1800, the monastery was enclosed by a stone fence. In 1810-1811, a three-tiered bell tower was added to the Holy Spirit Cathedral. In 1867, a stone church of the Sign of the Most Holy Theotokos was built.

In 1918, the Holy Spirit Monastery was closed and transferred to the military authorities. From May 1 to August 15, 1918, it housed the garage of the 23rd auto-armored detachment. By the summer of 1925, on the site of the demolished cemetery, which was hastily removed due to participation in the football championship of the RSFSR in 1924, the Dynamo stadium was built. Arguing with the authorities was futile. Almost simultaneously with the commission's decision, by the decree of the Vologda regional executive committee, the church of the Descent of the Holy Spirit and the chapel in the monastery were closed. Later, the building of the church and cells housed the regional administration of the NKVD and KGB of the USSR. The surviving cell block and the reconstructed cathedral belong to the Ministry of Internal Affairs.

After Perestroika, a memorial was established near the territory of the former monastery in memory of the victims of political repressions.