The Church of Archangel Gabriel with the chapel of Constantine and Helena was built between 1531 and 1534 simultaneously with the Church of the Beheading of John the Baptist at the order of Grand Duke Vasily III. In 1528, the duke, along with Duchess Elena Glinskaya, visited the monastery to pray for the birth of an heir. In honor of the birth of his son, the future Tsar Ivan the Terrible, he donated one thousand rubles to the Kirillo-Belozersky Monastery for the construction of two churches.

The architecture of this church and the Church of John the Baptist in the Ivanovsky Monastery reflects new elements introduced by Italian masters who worked in Moscow in the 15th and 16th centuries. The design of the facades and interiors was a novelty for stone construction in the early 16th century at the Kirillo-Belozersky Monastery. The facades of the Church of Archangel Gabriel are adorned with a profiled base and a wide three-part cornice. The upper part of the church, above the cornice, was decorated with walls of the second tier featuring large openings for bells, crowned with kokoshniks. A clock was placed in the northwestern corner of the tier. The church was topped with two domes: a large one in the center and a smaller one above the chapel of Constantine and Helena. In 1638, a sacristy with small windows and a vaulted ceiling was arranged in place of the bell tier. In the 18th and early 19th centuries, the monument suffered greatly: both drums were destroyed, the southern portal was demolished, replaced by new large windows, and the second tier of kokoshniks was destroyed. The western facade was almost completely covered by a stone bell tower. Of the three portals, only the northern one survived. In the collection of the Kirillo-Belozersky Museum-Reserve, only a few items of the church decoration have survived.

Restoration work on the monument has been carried out several times over the past decades. In the 1950s, specialists from the VPNRK studied and measured the monument, and architect S.S. Pod'yapolsky created a graphic reconstruction of its original appearance. In the 1960s and 1970s, conservation and partial restoration work was conducted, additional iron ties were installed in the arches between the pillars of the church, soil was partially removed from the eastern facade to improve water drainage, and the original base was restored. The late ceiling that covered the drum's throat was also slightly raised.