According to the chronicles of the Trinity-Sergius Lavra, in 1358, St. Sergius of Radonezh temporarily left the Trinity Monastery to find a place for a new monastery. At the Makhrish Monastery, he met with the abbot Stephen and took the monk Simon as his companion. After long wanderings, they settled on the high left bank of the Kirzhach River. Soon, Sergius' disciples joined them, and the brethren built cells and a wooden church in honor of the Annunciation of the Most Holy Theotokos. After living in the monastery on the Kirzhach for four years, Sergius returned to the Trinity Monastery, leaving his disciple, the venerable hieromonk Roman, as the abbot, who developed the Kirzhach Monastery until his death in 1392. Roman of Kirzhach, recognized as a saint, is considered the first abbot of the monastery.

Initially, the monastery was male and was under the administration of the Trinity-Sergius Lavra. In the 16th century, a stone church and a refectory church in honor of Sergius of Radonezh were built on the site of the wooden Annunciation church. In 1656, boyar Ivan Andreyevich Miloslavsky built the Spasskaya Church with a bell tower over the graves of his parents, and this place became the family burial site of the Miloslavskys. Archives indicate that in the Middle Ages, the monastery was surrounded by a stone wall, behind which, on the northern side, there was a chapel over the well dug by Sergius. In 1764, the monastery was abolished and transformed into the Blagoveshchensky parish. By the decree of Catherine II on the secularization of church property, the monastery's assets were transferred to the Trinity-Sergius Lavra, and the brethren were moved to other monasteries. In the mid-19th century, the founder of the silk industry in Kirzhach, Alexander Petrovich Solovyov, worked on the decoration of parish churches. In 1864 and 1869, his sons Pyotr and Alexander built the Church of All Saints with a tall bell tower. During the Soviet era, the monastery was inactive. In 1932 and 1934, the Church of Sergius of Radonezh was blown up. During the war, the Blagoveshchensky Cathedral was used as an ammunition depot, and later its premises housed a sausage workshop and a kerosene shop. The Church of All Saints housed the city bakery. Only in 1990 were the Blagoveshchensky and Spassky churches returned to the Russian Orthodox Church. In July 1995, by the decree of Archbishop Evlogy of Vladimir and Suzdal, the monastery resumed its activities as a women's monastery. In 1997, a reliquary with the relics of Roman of Kirzhach was installed in the basement of the Blagoveshchensky Cathedral. The Patriarch of Moscow and all Rus Alexy II attended the crowded services on the occasion of the discovery of the relics of Roman of Kirzhach.

Over the centuries, buildings in the monastery and around it were erected, decayed, and rebuilt, and many ancient structures, documents, icons, and wall paintings were lost over time. Of the surviving buildings, the architectural ensemble, which includes the Blagoveshchensky Cathedral and the Church of the Savior, is of particular interest. The four-pillar, single-domed Blagoveshchensky Cathedral has a tiered pyramid-shaped finish of kokoshniks, and inside, a system of arches and stepped vaults. The exact date of its construction is unknown, but the architectural forms allow it to be attributed to the early 16th century. The Church of the Savior was built in 1656 with the funds of boyar Ivan Andreyevich Miloslavsky as a family burial site, which is reflected in the strict architectural appearance of the building. The simple and clear square of the temple, standing on a basement, is topped with a tent-like bell tower instead of traditional domes. The Church of the Savior is connected by a platform with the Blagoveshchensky Cathedral, forming a single whole with it. Next to these churches is the Church of All Saints with a tall six-tiered bell tower, built in 1864 and 1869 in the neo-Russian style.