In 1755 two shrines, Hikawa Jinja and Dairokuten-Sha, were founded in what was then Itotani-Mura (伊藤谷村). The Kami at both shrines were revered as tutelar deities for the village, and both had the same betto-ji, the Shingon sect Yakushi-ji Temple.

Coming into the Meiji Period, Hikawa Jinja was given Village Shrine ranking, while Dairokuten-Sha’s name was changed to Koroku Jinja and it received no ranking.

In 1923 both shrines—which had been rebuilt in 1859, presumably because of the Ansei Edo Quake—were destroyed by the Great Kanto Earthquake and once again rebuilt. By 1971 both shrines were showing their age and prior to the necessary reconstruction Koroku Jinja was merged into Hikawa Jinja. Construction of a new shrine was begun in October 1973 in the Hiwaka Jinja grounds, and on October 10, 1975 the Kami was formally enshrined. It was at this time that the shrine was named Ayase Jinja.

Looking at the two in-ground shrines, Inari Jinja and Mitsumine Jinja, they are both formally subordinate shrines, the former to the old Hikawa Shrine, the latter to the old Koroku Jinja. The kami at Inari Jinja is  Uka-no-mitama-Kami, while Mitsumine Jinja enshrines three Kami, Yamato Takeru-no-Mikoto, and Izanami/Izanagi.