Tōfuku-ji was founded in 1236 by the imperial chancellor Kujō Michiie.[1] He appointed the monk Enni as founding priest, who had studied Rinzai Zen Buddhism in China under the monk Wuzhun Shifan. The temple was burned but rebuilt in the 15th century according to original plans. Tofuku-ji was one of the five temples of the Five Mountain System.

The temple was greatly reduced in size from 70 buildings to 25 during the Meiji era after the Shinbutsu bunri decree. In 1881, a fire burned down many major buildings such as the Main Hall, the Hōjo, the Hattō and the statue of Sakyamuni Buddha. During the Russo-Japanese War , the temple area was requisitioned and became a prisoner-of-war camp for Russians.

Both the main hall and the Hattō were rebuilt in 1917, and a new statue of Sakyamuni Buddha was later relocated to the temple in 1934.

In 1486 Ryōan Keigo became the 171st abbot of Tōfuku-ji. At the end of the 16th century Ankokuji Ekei was appointed abbot. From 1980 to 2009 Tōfuku-ji has been led by head abbot Keidō Fukushima.[2]