The church of Saint Vladimir, the Equal-to-the-Apostles Prince, was added to the northern side of the Assumption Cathedral. In 1554, at the initiative of the widow of Prince Vladimir Ivanovich, Maria Ivanovna from the Obolensky family, a church was built in honor of the Equal-to-the-Apostles Prince Vladimir over his grave. Subsequently, it became the burial place of the Vorotynsky princes. The construction of this church displeased Ivan the Terrible, who reproached the abbot Kozma and the brethren for building a church over Vorotynsky while there was none over the miracle worker. Although at that time it was not common practice to erect churches over the graves of private individuals, the monastery authorities allowed the construction because the prince and his wife made significant donations to the Kirillo-Belozersky Monastery. In 1554, the prince's widow transferred the village of Terebotun in Bezhetsk Upper, eight villages, and two wastelands to the monastery.

The Church of Vladimir is a small pillarless temple with a unique system of stepwise ascending arches. The external decoration of the church echoes the decor of the Assumption Cathedral, including three tiers of kokoshniks and stone ornamentation belts. The original appearance of the temple was altered: in the 18th century, it was covered with a gable roof, small arched windows were replaced with large rectangular ones, and the entrance from the north side was destroyed. The bulbous dome of the church is covered with wooden shingles, over which galvanized iron is applied for better preservation. On the forged base surrounding the dome from below, there is an inscription about the reconstruction of the dome in 1631. In 1997, for the 600th anniversary of the Kirillo-Belozersky Monastery, the dome and base were restored.