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In 736 the Buddhist monk Ennin, wishing to strengthen the protective function of the shrine dedicated to it an image he had carved of Zaō Gongen. By this time the shrine and the mountain had long been considered sacred by the Shugendo sects and the shrine was thereafter known as Mitake Zaogengon Jinja.

The main kami of the shrine, Kushimachi-no-mikoto, is something of a mystery. There is no reference to him in the Kiki, but Tanigawa (Japanese) points out that he was considered to be the jinushigami of the Mitake area and is often considered to be the kami of divination. He is also the major deity of the Amano-kaguyama Jinja in Kashihara, Nara-ken.

He is also known as Ōmatnotsu-no-Ōkami (大麻止乃豆乃大神), and in the Engishiki there is a reference to a shrine of this name in Musashi Tama-gun (武蔵国多摩郡大麻止乃豆乃天神社).  It is not clear exactly which shrine this refers to but there are thought to be three possible candidates, all sited close to the Tama River, Musashi Mitake Jinja, Marumiya-shinmei-sha (Tōkyō, Inagi-shi), and Ōkunitama Jinja (Tōkyō, Fuchū-shi). Along with the Shinbutsu Bunri in 1868 the first two of these shrines both petitioned to be recognized as the Shiki-nai sha and allowed to change their name to Omatonotsunoten Jinja. Marumiya-shinmei-sha was given the honour and is now known by the Engi-shiki name.

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Moving into the Kamakura Period, the shrine garnered substantial support from leading samurai, most notably Hatakeyama Shigetada. Among other things, he donated a suit of armour with red cords, which is now designated as a National Treasure, his saddle and long sword to the shrine. Around the turn of the twelfth century the shrine suffered war damage. In 1234, however, the 87th Emperor, Shijō, despatched an emissary, Ōnakatomi Kunikane (?, 大中臣国兼) to the shrine and he apparently had a vision of Mitake Gongen which inspired him to climb the mountain, and in addition to offering a new casting of Zaogengon he had the shrine rebuilt. In 1359 renovation work was sponsored by Ashikaga Motōji, and in 1511 the shrine was rebuilt with the support of the Mita clan. And then came the Tokugawa’s. In 1590 Ieyasu donated land yielding 30 koku per year, and in 1606 Ōkubo Nagayasu, a samurai at that time in the service of the Tokugawa Bakufu, oversaw reconstruction work which involved changing the direction in which the main hall faced from the south to the east to give spiritual protection to Edo Castle.

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Along with the Shinbutsu Bunri the Buddhist term "Zaogongen" was dropped from the shrine's name in 1874 and it became Mitake Jinja: in 1952 "Musashi" was prefixed to it and it became the Musashi Mitake Jinja, the name which it still bears.