The vast compounds of Chion-in include the site where Hōnen settled to disseminate his teachings and the site where he died.
The original temple was built in 1234 by Hōnen's disciple, Genchi (1183–1238) in memory of his master and was named Chion-in. While the temple was affiliated more closely in the early years with the Seizan branch of Jodo Shu, its 8th head priest, Nyoichi (1262–1321) was deeply influenced by the priest Ryōkū, a disciple of Ryōchū who was the 3rd head of the Chinzei branch of Jodo Shu Buddhism, and disciple of Bencho. Later Nyoichi's successor Shunjō (1255–1355) advanced this further by citing a biography where Genchi's disciple Renjaku-bo and Ryōchū agree that there existed no doctrinal differences between them:
By 1450, Chion-in had become fully under control of the Chinzei branch, but had little direct control, due to the outbreak of the Onin War. Numerous buildings in the complex were burnt down in 1633, but were entirely rebuilt by the third Tokugawa Shogun Iemitsu (1604–51) with the palatial structures that stand today.Then Renjaku-bo said, "There is complete agreement between what Genchi and Bencho say in their basic teaching. So my disciples should from now on look at the Chinzei teaching as their own. There is no need to set up another school."