It is part of the Rinzai school of Zen's Engaku-ji branch, and was opened by Hōjō Sadatoki and founding abbess Kakusan-ni in 1285.

The temple was founded in the 8th year of Koan (1285) by nun Kakusan-ni, wife of Hōjō Tokimune (1251–1284) and mother of Sadatoki, after her husband's death.

The temple remained a nunnery for over 600 years and men could not enter until 1902, when a man took the post of abbot and Tōkei-ji came under the supervision of Engaku-ji.

Tenshū-ni, the daughter and only survivor of Toyotomi Hideyori's family, son of Hideyoshi, entered Tōkei-ji following the Siege of Osaka.

The temple's old Butsuden, an Important Cultural Property, was bought during the Meiji period by businessman Tomitaro Hara and is now in the garden he built, Yokohama's Sankei-en.