During the late Nara period and early Heian period, after the establishment of a centralized government under the Ritsuryō system, the imperial court sent a number of military expeditions to what is now the Tōhoku region of northern Japan to bring the local Emishi tribes under its control.

During the Kamakura period, under the sponsorship of Hōjō Tokimune, the temple changed from Tendai to Zen, with Rankei Dōryū has its head priest and came to a patronised by the samurai class.

During the Edo period, it was rebuilt by Date Masamune from 1604 onwards using lumber brought from Mount Kumano in what is now Wakayama Prefecture and skilled workmen from Kyoto and Kii Province.

The haiku poet Matsuo Bashō wrote a tribute to the golden walls inside the temple.

The temple grounds also contain the Zuigan-ji Art Museum established on October 1, 1995, to display various artifacts, including calligraphy by former head monks, fusuma paintings, tea cups and portraits.