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The monastery was founded in 1548 by Fyodor Syrkov, a wealthy merchant whose family built several churches in Novgorod. The eldest brother, Ivan Syrkov, erected the Church of the Holy Myrrh-Bearing Women in Yaroslav's Court in 1510. His son Dmitry sponsored the Chapel of St Varlaam at Khutyn Monastery. But Fyodor was the most active member of his family when it came to building churches. Fyodor Syrkov served as a diplomatic official in Moscow. One of his missions was to head a dangerous embassy to the Baltic lands, so he vowed to build a monastery in Syrkovo with a church in honour of the Vladimir Mother of God if he survived. A stone votive cathedral was erected at the monastery through his efforts in 1552-1554 – an imposing cube-shaped four-pillar triconch building with a lower western narthex.

According to the early 20th century descriptions, the floor in the altar part and in front of the iconostasis was tiled with ancient bricks fastened with lime and placed on pots filled with sand.

There is a restored commemorative plate and a cenotaph outside the Vladimir Cathedral honouring Vera the Silent, an Orthodox hermit cloistered at the Syrkov nunnery who kept a vow of silence for 23 years.

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