According to chronicles, in the first half of the 14th century, Metropolitan Peter received from Grand Duke Ivan Kalita a plot of land north of the Assumption Cathedral in the Kremlin for his court.

In 1450, Metropolitan Jonah built a stone church of the Transfiguration and the first stone chamber in the Kremlin on this site. After the Moscow fire of 1473, Metropolitan Gerontius rebuilt the court. In 1484-1485, Pskov masters erected a new church of the Transfiguration, which has survived to this day. All subsequent metropolitans, and from the late 16th century, patriarchs, continued to develop their holdings in the Kremlin, constructing wooden and stone buildings.

During the Polish-Lithuanian intervention and the fire of 1626, the Patriarchal court suffered from the flames. Patriarch Filaret restored the Cross and Dining chambers, as well as built wooden cells and churches.

In 1643, a new phase of construction began under Patriarch Joseph. The Cross, Golden, Cell, and Treasury chambers, as well as auxiliary premises, were erected under one roof. The works were led by Antipa Konstantinov, who participated in the construction of the Terem Palace.

The next phase in the history of the patriarchal court is associated with Patriarch Nikon. In the autumn of 1652, the dismantling of the old chambers and buildings on the former court of Boris Godunov began, which Nikon received as a gift from Tsar Alexei Mikhailovich. By the end of 1655, new chambers and a church were built, and the finishing of the premises continued until July 1658, when Nikon left the see. The first floor of the palace was used for economic needs, the second housed the ceremonial halls and the household church, while the third contained the personal quarters of the patriarch.

Subsequent patriarchs also made changes to the architecture and decor of the palace.

In 1721, after the abolition of the patriarchate and the creation of the Holy Synod, the building housed its Moscow office, which led to significant changes in the layout and decoration of the chambers.

In 1918, the Patriarchal chambers, as a unique architectural monument of the 17th century, were transferred to the museum. A long scientific restoration began, during which the building regained its original appearance. In 1967, the first permanent exhibition was opened on the second floor of the Patriarchal chambers.

In 1980 and 1985, major scientific restoration works were carried out, resulting in the modern exhibition of the museum.

In the 2010s, the museum's exhibition was somewhat altered. During renovation work in 2013, sections of 17th-century paintings on the walls of the ceremonial halls and command chambers were uncovered.