In the seventh month of 1335, Hojo Tokiyuki (?–1353), son of the last effective Hojo regent Takatoki, raised an army with the support of Suwa Yorishige of Shinano Province in what became known as the Nakasendai Rebellion. As Tokiyuki's forces advanced on Kamakura, Ashikaga Tadayoshi — defending the city — feared that the imprisoned Prince Moriyoshi might be freed and used as a rallying point. He ordered his retainer Fuchibe Yoshihiro to execute the prince. Ironically, Tokiyuki's advance was the direct trigger for Moriyoshi's death. Tokiyuki briefly retook Kamakura but was driven out within about two weeks by Ashikaga Takauji, who then broke with Emperor Go-Daigo. Tokiyuki continued fighting for the Southern Court in subsequent years, never abandoning hope of Hojo restoration.

Kamakura-gu was founded in 1869 by imperial decree on the very site — the former Tokoji Temple — where Prince Moriyoshi was imprisoned in a dungeon for some nine months and executed on July 23, 1335, on the orders of Ashikaga Tadayoshi. Moriyoshi is the shrine's sole object of worship. The dungeon behind the main hall is the actual place of his imprisonment; the treasure hall holds surviving imperial proclamations and a mounted statue of the prince. The Taiheiki's account of Moriyoshi biting through the assassin's blade — resisting even at the moment of death — made him the symbol of unwavering loyalty to the imperial cause that the Meiji government sought to enshrine as a national ideal.