The most notable structure at the fort, the chapel, is unusual for North America and often photographed. With its landmark "small belfry" a familiar sight along Highway One, the chapel is a mecca to visiting Russians. The greatest efforts made over the years in maintenance and preservation at Fort Ross have been for the chapel. It was constructed by the resident Russians about 1825 with their own funds, and funds donated by visiting Russian officers and crew of the Kreiser. The chapel was never consecrated and there was no permanent priest; but one Company official, Fedor Svin'in, appeared to act as a lay deacon, according to Father Payeras. It was used and revered during the Russian tenure, as it is today. "The chapel with a cupola," as it appears in the Russians' inventory for Mr. Sutter in 1841, is not anywhere extensively described by early visitors to the fort. The earliest photographs of the original Russian chapel are from the 1880s.

In the 1906 earthquake the chapel's old walls completely caved in and the floors and foundation were reduced to rubble. The roof and the turrets came to rest over the foundation virtually intact. In the spring of 1916 the State Legislature appropriated $3,000 toward its reconstruction. George W. Call's son, Carlos, a strong advocate of the proposal, was appointed supervisor of the rebuilding. The chapel's reconstruction mainly involved giving the building a new foundation and walls and bringing the original roof into position. Carlos Call and his local carpenters solved the practical problems of increasing the building's structural integrity, but the chapel's original appearance was changed.

To replace the building's broken supports, original Russian-cut timbers and planks were taken from the officials' quarters and part of the old warehouse. Since the upright wallboards from the officials' quarters were over a foot too short for the chapel walls, the floor was raised to make the chapel roof the correct height. It was then necessary to add a small porch and step to the front of the chapel to make it easier to enter. From historic measurements and observations of similar chapels in Russia, such an addition was reasonable, and in fact there once may have been an extended shed-roofed porch or kryltso, typical in similar Russian chapels. Due to the damage sustained by the ceiling joists and roof beams, an extra side wall stud was added for stronger support. This increased the number of panels on the south wall, and thus the number of windows, from three to four. Later it was found that in this 1916-18 reconstruction the north and east walls of the chapel were not aligned with the original stockade; this was subsequently corrected.

A serious error with theological implications occurred when the roof of the cupola was restored in a different style and a Roman, rather than Russian Orthodox, cross was erected on the bell tower. In 1939, a Russian Orthodox cross replaced the Roman cross; however, it was put on the bell tower upside-down due to a carpenter's misinterpretation of a pattern given to him by a visiting Russian Orthodox bishop. A letter to the governor of California signed by several hundred people noting the mistake was forwarded to the carpenter, and in 1941 the Russian Orthodox cross was put up correctly!

Although the Park staff was aware of the changes in design and recommended their correction, the alterations produced by the 1916 reconstruction remained for nearly forty years. Only as public interest in Fort Ross grew and the study of its building construction became more intensive, was the state persuaded to appropriate new funds to bring the building into closer conformity with the original. Finally, in 1955, a second restoration was funded. The walls of the chapel were rebuilt with three windows and the building was correctly aligned with the adjoining stockade as indicated by archaeological excavation, but the elevation of the floor was still high. In 1960, the cupola was replaced with a more authentic Russian roof style, and a small cross was added. This cross was later replaced by a tall Russian Orthodox cross.

On October 5, 1970, the restored Russian chapel was entirely destroyed in an accidental fire that swept through the building, leaving nothing but a few charred timbers. Once again supporters of Fort Ross quickly organized to promote a third rebuilding of the chapel. Funds were obtained from a variety of sources; local residents, Russian American groups, and government agencies all contributed. The Department of Parks and Recreation conducted a comprehensive study of the building site based on new archaeological techniques, and developed updated historical data and additional detail on floor alignment, configuration, and use of building materials. The chapel that emerged in 1973 is what is seen today in the compound.

When the Russians left Fort Ross in 1841, they apparently took all the icons with them. They left one large bell, a candelabra, a candlestand and a lectern which were destroyed when the chapel burned in 1970. All have been replaced with replicas. The bell that hangs today outside the rebuilt chapel was recast, using the original bell's materials and a rubbing which had been made from the original. It bears the inscription: "Cast in the St. Petersburg Foundry of Master Craftsman Mikhail Makharovich Stukolkin." The bell's deep, resonant chime can easily be heard across the stockade, and twice a year it announces to the public the Orthodox services held in the chapel.