One of the "Three Ayase Jinja," its affairs are managed by Ayase Inari Jinja, In August 1504 a monk by the name of Kensora (?) attached to the Shingon sect Buddhist temple Yakuōyama Hōmochiin Shinzen-ji in Kasa Aoto village founded another temple called Yofuku-ji in Fugenji Village, now part of Ayase. Four shrines—Inari-Sha, Tenjin-Sha, Dairokuten-Sha, Hachiman-Sha—were built on land adjoining Yofuku-ji. Inari-Sha and Tenjin-Sha were later merged, Dairokuten-Sha and Hachiman-Sha were moved and became auxiliary shrines of the Inari/Tenjin entity, which was then given the name Kitano Jinja. The new shrine became the tutelary deity for the entire Yofuku-ji parish.

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In October 1855 much of the shrine was destroyed in the Ansei Edo Earthquake: the main hall was rebuilt and a building record dating from September 1862 indicates that much other repair and reconstruction work was being carried out. In 1977 the Main Hall was greatly expanded and in 1995 the Prayer Hall was reconstructed.

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