John W. Ashton earned both his B.A. and Doctor of Laws degrees from Bates College. He earned his Doctor of Philosophy degree from the University of Chicago in 1928. He began his teaching career at Indiana University (IU) in 1946 as a professor of English and Dean of the College of Arts and Sciences. He was later made Vice President and Director of Student Educational Services, a new position, and in 1958 he was named Dean of the Graduate School and Vice President for Graduate Development.
Before joining the IU faculty, Ashton served as a faculty member at Yankton College, the University of Iowa, and the University of Kansas. Directly before coming to Indiana University, he took one year off to serve as Head of the United States Army University in Shrivenham, England.
Upon his retirement from IU, Ashton was granted the title of University Professor of English and Folklore. Earlier in his career, in 1932-33, he was awarded an International Research Fellowship at the Huntington Library, and the promise shown by this recognition was fulfilled not only by a myriad of publications in the usual journals but also by subsequent work performed by doctoral candidates who studied with him and wrote their dissertations under his guidance.