The Church of the Intercession of the Holy Virgin, located next to the Transfiguration Church and forming a unified ensemble with it, was built 50 years later than its "neighbor." Its construction began in 1694, shortly after a fire destroyed the previous churches of Kizhi Pogost. However, in the following century, in 1764, the church underwent significant reconstruction, acquiring its modern forms and proportions. The craftsmen aimed to create a structure that would harmonize with the main church of Kizhi Pogost, the Transfiguration Church, matching it in splendor and not getting lost against its backdrop.

In the 1860s, during repairs, the Intercession Church was clad in planks, which were only removed in the late 1950s thanks to restoration carried out under the project of Moscow restorer A. V. Opolovnikov. In 1865, the church lost its Nikolsky chapel, which was dismantled due to overcrowding. The main part of the church is an octagon on a square base, covered with an eight-pitched roof with small domes on the smaller octagons. Eight small domes are grouped around a larger ninth, giving the church's completion the appearance of a crown. This octagon on a square base unites the altar with an additional dome, the refectory, the vestibule, and the porch into a single complex.

Since the 17th century, when zemstvo activity intensified in Russia and local self-government strengthened, refectories became almost an obligatory part of winter churches. In the refectory of the Intercession Church, where the residents of the pogost gathered, pressing matters were discussed, court hearings were held, royal and voivode decrees were announced, and officials were elected. Later, church parish school classes were held here. Benches are arranged along the walls of the refectory, and stoves are located in the corners. Currently, a small exhibition dedicated to the Kizhi Uprising of 1769-1771 is located in the vestibule. The porch of the church, in its design and decorative details, resembles the porches of peasant houses, differing in simplicity and expressiveness. Many features connect this church with civil buildings: the log cabin construction "in oblo," a high underfloor, and a nail-free roof with eaves, gables, and a towel. The interior decoration of the church has changed multiple times.

The renovation of 1903 was particularly significant, when the walls of the church were plastered and painted with oil paint, with the lower part imitating a marble base. At that time, the ceilings were also plastered and decorated with stucco cornices. The windows were enlarged, and the wall separating the refectory from the church space was almost completely cut out. In the 1950s, the interiors of the church were restored according to A. V. Opolovnikov's project, largely returning to their original appearance; however, it was not possible to completely eliminate traces of plaster, which are still visible today.

The recreation of the interior in the 1960s was carried out by Galina Ivanovna Frolova, a researcher at the Kizhi Museum-Reserve, a tempera painting restorer, and a museum collection of icons. The iconostasis in the church is assembled, composed in 1956-1959 from icons of Zaonezh painting from the 17th-19th centuries. Today, the winter Church of the Intercession of the Holy Virgin houses a four-tiered tabernacle iconostasis, reconstructed by Opolovnikov based on a scheme developed in 1948 by V. G. Bryusova Svetlichnaya. The earliest icons, dated to the second half of the 17th century, were selected for the iconostasis from the "Kizhi Collection," composed of Zaonezh icons that were taken to Finland during the occupation. The original iconostasis has not survived; it is only known that it was also a tabernacle. A small exhibition titled "Ancient Russian Painting of Karelia" from the collections of the Kizhi Museum-Reserve is located in the church. The height of the church is 26 m, its total length is 32 m, and its width is 8 m. The materials used are pine and aspen.

Currently, the Intercession Church is used jointly by the Russian Orthodox Church and the museum. Previously, the "winter" church was heated, and services were held in it from October 1 until Easter. Worship services have been held again in the summer since 1997.