Hunter returned to New Zealand to begin his academic career. He was a lecturer in bioorganic chemistry at the University of Otago from 1989 to 1991. He then returned to the United Kingdom and joined the University of Sheffield. He was a lecturer from 1991 to 1994 and reader from 1994 to 1997. He was promoted to professor of chemistry in 1997. He held a Lister Institute Research Fellowship from 1994 to 1999, and an Engineering and Physical Sciences Research Council Senior Research Fellowship from 2005 to 2010.
In September 2013, he was selected as the next Herchel Smith Professor of Organic Chemistry. He joined the University of Cambridge in early 2014 to take up the appointment. There, he is a member of the Synthetic Chemistry Research Interest Group. He is also a Fellow of Emmanuel College, Cambridge.