Dr. Winterton began his career in the early 1960s working for the Bureau of Indian Affairs on the Navajo Reservation in New Mexico. There, he taught school before being named principal of the Lake Valley school near the Chaco Culture National Historical Park. His final assignment on the Navajo was as principal of the Dzilth-na-o-dith-hle Elementary/Junior High school near Huerfano Mesa, one of the six sacred landforms in Navajo mythology.
Following his Navajo years, he served as the Administrator of the Albuquerque Indian High School, Superintendent of Schools for the Northern Pueblos Agency, and President of the Institute of American Indian Arts, a junior college in Santa Fe. In 1986 he transferred to Phoenix, Arizona, where he completed forty-plus years of federal service at the Bureau of Land Management's National Training Center, retiring in 2004.