Born in 1937, John White was of Shawnee, Cherokee, and Scots descent, as well as a descendent from the son of Ten-ska-wa-ta (Tecumtha's brother often known as The Shawnee Prophet) who stayed for several years (1811-1814) with his Cherokee ancestors, the family of Elijah Hicks in the Sequachie Valley of Tennessee. There, White's ancestors were from the Chicamauga Band of Cherokee, who continued to fight against the colonists after 1776 when the Cherokee Nation was defeated. The most prominent member of White's lineage from this time was Dragging Canoe, Tsiyu-gun-su-ni, the principal war leader of the Loyalist faction. While the Cherokee Nation did not join Tecumtha's movement many young men of the Chicamauga Band fought with him.

Throughout his lifetime, White served as a cultural preservationist, historian, storyteller, and teacher in many capacities. Many of the oral traditions White retold he heard first from his great uncles and Great Aunt Sally Hicks, who all spoke Cherokee. He attended Bacone Indian College, now Bacone College, in Muskogee, Oklahoma for one year before serving in the Army for four years in post-war Korea. Upon his return to the United States, he took courses at the School of the Art Institute of Chicago, and then finished his baccalaureate course work at the California College of Arts and Crafts, now the California College of Arts, in 1968. There, he majored in ceramics with a minor in art history. In 1970, he completed a divisional M.A. at the University of Chicago, where he combined anthropology, education, history, and political science to create a program more relevant to American Indian education. After his time at the University of Chicago, he attended Stanford University, where received a M.A. in anthropology. He worked at the Field Museum of Natural History from 1973-1976, as the Native American Outreach Program Director and as the Pawnee Earth Lodge Project Director. He then served as the Sacred Circles Exhibition, Educational and Cultural Programs Director at the Nelson-Atkins Gallery in Kansas City, Missouri from 1976-1977. After that, from 1978-1985, he worked as the Ethnographic and Experimental Archaeology Studies Program Director for the Center for American Archaeology in Kampsville, Illinois. In 1985, he and his wife, Ellanor "Ela" White, founded the Ancient Lifeways Institute in Michael, Illinois. At the Ancient Lifeways Institute, he built Scottish and Indian villages where students from around the country came to learn the crafts, foods, languages, and stories of his ancestors. John and Ela often ran the field school with their children Karli, Mark, Jonah, and Watie.

In 1974, White interviewed elderly residents of Calhoun County about stories they may have heard about Indians in the area for Northwestern University's archaeological program. Through this particular project, John met Gerhard Cappel who could still speak the native language he learned as a child. In 1987, William "Bill" Cappel, Pirushi Makwa, The Far Off Bear, and Chief of the Tamaroa and Metchigamea Tribes of Illinois, Gerhard's oldest son, decided to revive certain aspects of Illiniwek culture, and so he appointed White to be his assistant or Akapia. In his position as Cappel's Akapia, White got involved in teaching Illiniwek culture and language at local public schools. In 1996, when Bill Cappel stepped down as Chief, he appointed White to take his place.

In 1994, members of the congregation of the Church of the Immaculate Conception on Kaskaskia Island requested assistance with efforts to prevent the church's closure, and John and Ela got involved. Some of the results included a revival of the traditional naming ceremony and the reintroduction of Illiniwek prayers and hymns in the church services.

White died on July 7, 2006 of pancreatic cancer.