The construction of the Annunciation Cathedral began under the guidance of St. Seraphim, who said that another church should be built in the monastery, aligned with the bell tower and the Trinity Cathedral, at the end of the Holy Canal. On April 26, 2012, Metropolitan Georgy held a prayer service in the Trinity Cathedral to bless the start of this good work.

According to the project, the dimensions of the church were determined by the Belt of the Virgin: twenty belts in width, thirty in length, and fifty in height, totaling 60 meters. The design was based on the church of the Moscow Zayikonospassky Monastery, executed in a style close to Moscow Baroque of the early 18th century. The new cathedral became snow-white, with a steel-colored roof and a golden dome. It was planned to create eight chapels, and the main altar was consecrated in honor of the Annunciation of the Holy Virgin.

Preparation for the construction of the cathedral lasted more than ten years, during which a project competition was held, necessary documents were prepared, and the construction site was readied. On August 27, 2015, on the eve of the Dormition of the Holy Virgin, the chapel of the new cathedral was consecrated. The Rite of the Great Consecration of the first chapel of the church was performed by Metropolitan Georgy of Nizhny Novgorod and Arzamas. On November 17, 2016, the chapel in honor of the appearance of the Mother of God to St. Sergius of Radonezh was consecrated, and this ceremony was also led by Metropolitan Georgy. He was assisted by Metropolitan David of Alaverdi, Bishop Benjamin of Ardatov and Atyashevo, and Bishop Vasily of Kotlas and Velsk. Metropolitan Georgy recalled how, while studying in Moscow spiritual schools, he read the chronicle of the Diveyevo Monastery and regretted that he could not walk along the Holy Canal and venerate the relics of St. Seraphim of Sarov. However, 25 years ago, the revival of the monastery began, and now it can be seen in all its glory. The bishop emphasized that the consecration symbolizes the connection between the heavenly and earthly Church. When St. Seraphim was buried, an icon of the appearance of the Queen of Heaven to St. Sergius was placed in his coffin.

On May 11, 2019, Metropolitan Georgy consecrated the chapel of the Annunciation Cathedral in honor of the Resurrection of the Word, and on the same day, the first liturgy was held in the new chapel.