He graduated in 1950 from the Tokyo National University of Fine Arts and Music and began working in documentary film.
He is best known for his films Woman in the Dunes and The Face of Another. He directed his first feature film, Pitfall (1962), in collaboration with author Kōbō Abe and musician Toru Takemitsu. In 1972, he worked with Japanese researcher and translator John Nathan to make Summer Soldiers, a film set during the Vietnam War about American deserters living on the fringe of Japanese society.
From the mid-1970s onwards, he worked less frequently on feature films as he concentrated more on documentaries, exhibitions and the Sogetsu School and became grand master of the school in 1980.
In 1978, Teshigahara directed the final two episodes of the long running and popular Japanese television series Shin Zatoichi, starring Shintaro Katsu as the blind wandering Yakuza. During Akira Kurosawa"s five-year hiatus from filmmaking, he watched a lot of television and was particularly taken by the final episode of Shin Zatouichi - Episode: Journey of Dreams (新座頭市「夢の旅) (1978).
The influence of this particular episode included the initial casting of Shintaro Katsu in the lead roles in Kagemusha (1980) and the extended artistic dream sequences contributed to those seen in Kagemusha. On the first anniversary of his death, April 14, 2002, a Digital Video Disc box set containing his best known work was released in Japan in commemoration.