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Studi appeared in his first film, The Trial of Standing Bear, in 1988. He is known for his roles as ruthless Native American warriors, such as a Pawnee in Dances with Wolves (1990), and the Huron Magua in The Last of the Mohicans (1992).
A year later, he was cast with Eric Schweig for TNT's film The Broken Chain, about the historic Iroquois League that was based in the area of central and western present-day New York state. It was shot in Virginia. This was part of a group of productions shown over 14 months on TNT as its "Native American initiative", including three television movies and several documentaries. A six-hour history series was told from a Native American perspective. In 1993 Studi had the lead in Geronimo: An American Legend. He played the superhero Sphinx in the 1999 comedy film Mystery Men.
In 2002, Studi brought to life the character of Police Lieutenant Joe Leaphorn, for a series of PBS movies based on Tony Hillerman's novels set in the Southwest among the Navajo and Hopi. It was produced by Robert Redford. Some movie titles include "Skinwalkers", "Coyote Waits", "A Thief of Time".
In 2005, Studi portrayed a character based on chief Opechancanough, leader of the Powhatan Confederacy in Virginia, in the film The New World directed by Terrence Malick.
In 2009, Studi appeared as Major Ridge, a leader of the Cherokee before the Native American removal to Indian Territory, in Trail of Tears. This was the third of five episodes in the PBS series We Shall Remain, portraying critical episodes in Native American history after European encounter, part of the public television's acclaimed series American Experience, where Studi spoke only in native Cherokee.
Also in 2009, Studi appeared in James Cameron's Avatar. He played Eytukan, the chieftain of a Na'vi tribe, but did not have any dialogue in English. Studi played Cheyenne chief Yellow Hawk in a starring role in the 2017 film Hostiles.
At the 90th Academy Awards, Studi introduced a tribute to military movies, and gave part of his speech in the Cherokee language, of which he is a fluent speaker. Studi is the second Native American actor to present at the Academy Awards. Will Rogers hosted in 1934.
In 2019, he received an Academy Honorary Award, becoming the second Indigenous person to be honored, and the first Native American actor to receive an Oscar specifically for acting. In his acceptance speech, Studi said: "I’d simply like to say, it’s about time. It’s been a wild and wonderful ride, and I’m really proud to be here tonight as the first Indigenous Native American to receive an Academy Award. It’s a humbling honour to receive an award for something I love to do." The first Indigenous person from North America to win an Oscar was Buffy Sainte-Marie, a First Nations/Native American living in Canada, in 1983, for Best Original Song at the 55th Academy Awards.