According to the life of St. Cyril of Belozersk, the wooden chapel was built by Cyril himself when he arrived at Belozero in 1397. The modern structure is later, but likely retains the overall architectural style of the late 14th century. Dendrochronological studies conducted in the 1980s showed that the wood of the chapel was harvested no earlier than the 18th century. Various elements of the log structure, roof, and openings likely belong to different periods. The presence of metal details, such as supports and door fittings, as well as nails, from wrought to modern, indicates repairs made over the centuries. The chapel housed three wooden crosses, one of which is now displayed in a museum. Dendrochronological analysis of the crosses, also conducted in the 1980s, dates them to the first quarter of the 17th century.

The Chapel of Cyril represents a traditional type of small chapels common in Northern Russia. Its forms are simple and concise, giving the structure a severe ascetic appearance. This wooden building is an interesting but still insufficiently studied monument of wooden architecture.

In the late 18th century, a stone canopy was erected over the chapel for protection against the weather. Its architecture is similar to the stone canopy over the cross, indicating that they were likely created according to the same design. The restoration of the canopy was carried out in 1994.