Zvenigorod rose to prominence in the late 14th century, after it was bequeathed by Dmitry Donskoy to his second son Yuri, who founded his residence on the steep bank of the Moskva River. The local kremlin, called Gorodok, contains the only fully preserved example of 14th-century Muscovite architecture, the Assumption Cathedral (1399). The cathedral's interior features frescoes by the great Andrei Rublev.
Zvenigorod is primarily remembered for internecine wars waged by Yuri's sons for control of Moscow during the reign of their cousin Vasily II (1425–1462). After their party was defeated, the town was incorporated in Muscovy.
Zvenigorod was granted municipal rights in 1784. By the late 19th century, the town gained popularity among intelligentsia as a fashionable banlieu of Moscow. Many extravagant dachas were built in the neighbourhood. Some of these house museums of Sergey Taneev, Anton Chekhov, and Isaac Levitan.
In 1398, Prince Yuri asked St. Savva, one of the first disciples of Sergii Radonezhsky, to go to Zvenigorod and to establish a monastery on the Storozhi Holm (Watching Hill). St. Savva of Storozhi was interred in the white stone cathedral of the Virgin's Nativity in 1407. This diminutive, roughly hewn church still stands, although its present-day exquisite look is the result of recent restoration. The frescoes in the altar date back to the 1420s, but the rest of interior was painted in 1656. A magnificent iconostasis in five tiers and the Stroganov-school heaven gates were installed in 1652.
In 1650, the monastery was chosen by Tsar Alexis as his suburban residence. In five years, they constructed a white-stone royal palace and a festive chamber for tsaritsa. The cloister was encircled with stone walls and towers, patterned after those of the Troitse-Sergiyeva Lavra. Particularly noteworthy is a large belfry, erected in four bays in 1650 and crowned with three tents and a clocktower. A church over the holy gates was consecrated to the Holy Trinity in 1652.
After the death of Feodor III, who spent most of his time there, the monastery declined. In May 1918, when the Bolsheviks tried to seize the relics of St. Savva, several persons were shot dead. In 1985, the cloister was assigned to the Danilov Monastery in Moscow. St. Savva's relics were returned to the monastery in 1998.