He began his career in academe as a member of the faculty at the University of Kentucky, where he taught mathematics for five years.
He left Chattanooga in 1979 to become vice president for academic affairs, dean of the faculty, and professor of mathematics at Susquehanna University in Pennsylvania.
In 1984 he was named president there where he remained until 2000, when he was elected vice chancellor by Sewanee's board of trustees and made his second Tennessee homecoming.
Cunningham presided over the celebration of the sesquicentennial anniversary of the university's founding in 2007–08, which coincided with the end of the successful capital campaign and the dedication of the state-of-the-art science building Spencer Hall.
During the final year of Dr. Cunningham's service, a major renovation and addition to Snowden Hall took shape as a new home for the forestry, geology and natural resources departments.