Hexter was a 1974 magna cum laude graduate of Harvard College and a member of Phi Beta Kappa. After studying in England at Oxford's Corpus Christi College, he entered graduate school at Yale University. He received his Masters of Philosophy in 1979 and his Ph.D. in 1982 both from Yale and taught there in Classics and Humanities for ten years.
He was professor of classics and comparative literature and director of the graduate program in comparative literature at the University of Colorado at Boulder. His first faculty appointment was at Yale University, where he taught for 10 years and was director of undergraduate studies in the humanities major, also serving for one year as acting associate dean of the graduate school.
Hexter then was Executive Dean of Letters and Science and Dean of Arts and Humanities and at University of California, Berkeley. Hampshire is part of the five college consortium, which includes Mount Holyoke College, Amherst College, Smith College, and the University of Massachusetts Amherst.
Hexter assumed the Hampshire College presidency on August 1, 2005. He is the the fifth president of Hampshire College, a progressive alternative college in Amherst, Massachusetts.
As is required of a president by Hampshire's constitution, Hexter is technically a full-time professor with given specialities in Classics and Literature. He is one of the few openly gay college presidents in America. When Ralph Hexter assumed the presidency of Hampshire College in western Massachusetts in 2005, his partner of 25 years, Manfred Kollmeir, was officially welcomed with all the trappings of a presidential spouse.
On September 18, 2007, a "Critical Announcement" was released to the Hampshire College students by President Hexter. In it, he states:
"As most of you know, many years ago Manfred and I made a lifelong commitment to one another. Today we are excited to share with you the news that we were married over the Labor Day weekend.
When we arrived at Hampshire College in August 2005, we were deeply touched by the warm reception we received from the community and continue to feel honored to be a part of a group that embraces and celebrates diversity. We appreciate that living in Massachusetts has afforded us the same rights as any other couple. By choosing to be legally married we want to send a strong message that we believe discrimination should end everywhere and that all couples who wish to marry should have the right to do so."
The message went on to invite the students to celebrate the happy occasion with President Hexter and Manfred Kollmeier in an on-campus reception.