In November 1591, Tokugawa Ieyasu issued a red-seal certificate (shuinjo) granting Enmeiji 5 koku of temple land. Having long served as a prayer temple for both the Miura and Go-Hojo clans, Enmeiji was among the temples favored by Ieyasu in his consolidation of religious institutions across the Miura Peninsula soon after his entry into the Kanto, and it endured throughout the Edo period as a shuin-ji (red-seal temple).

During his travels through the provinces in the Tenpyo era (729-749), the monk Gyoki is said to have visited Zushi, carved a seated Enmei Jizo Bosatsu by his own hand, and founded Enmeiji. One of the greatest monks of the Nara period, Gyoki led public works across Japan — bridges, reservoirs, charitable halls — and was later invited by Emperor Shomu to help build the Great Buddha of Todaiji. Temple tradition holds that his wish 'to prolong the lives of all people and to relieve their suffering' was embodied in the Jizo image preserved here.

As a Koyasan Shingon temple, Enmeiji transmits the esoteric teachings of Kobo Daishi (Kukai), and its popular name 'Zushi Daishi' derives from the devotion to him. On the 21st of each month — Daishi's feast day — many Zushi residents come to worship, continuing the Daishi-ko tradition that has been observed since the Edo period. The Shingon teachings founded by Kukai merged with this ancient Gyoki-founded temple to shape the religious culture of the area.