The monastery was founded in 1689 on the right bank of the Angara River. The original buildings were wooden, and by 1727 the Cathedral of the Znamenka Church, built in 1693, had become dilapidated. In 1762, the monastery was rebuilt in stone, and the chapels and other structures were completed over the following years.

On the night of February 6-7, 1920, the Supreme Ruler of Russia, Alexander Kolchak, and the Chairman of the Council of Ministers, Viktor Pepelyaev, were shot near the monastery. After the arrival of Soviet power in Irkutsk, the local diocese was left with only the church building, and the monastery was closed. Its premises housed departments of hydroaviators, and from 1928, the Irkutsk hydroport was located at the mouth of Ushakovka.

In 1926, the Znamenka Church became a parish church, and from 1929 it began to serve as a cathedral, as the Epiphany Cathedral was completely closed for religious needs, and the Kazan Cathedral was demolished. Seven years later, the Znamenka Church was closed again, and its buildings were used for aircraft repair workshops and garages.

With the onset of the war, the Irkutsk hydroport ceased passenger transport, and pilots and planes were mobilized. Only the hydroplanes of the NKPS remained at the monastery, which serviced the BAM. In 1945, the Znamenka Church was returned to the diocese, and in 1948 it regained the status of a cathedral. In 1953, the NKPS hydroplane base was closed.

On August 30, 1960, the Znamenka Monastery complex was recognized as a monument of architecture of republican significance and placed under state protection.

Since 1991, the relics of Saint Innocent Kulchitsky have been located in the Znamenka Church, and on August 27, 1994, the monastic tonsure was revived in the monastery. Currently, the diocesan administration of the Irkutsk Metropolis is located on the monastery grounds.