Hunter was born on 30 October 1953.^[2] He grew up in Australia, and was educated at Cranbrook School, an independent school in Sydney.^[2] He studied at the University of Sydney, graduating with a Bachelor of Arts (BA Hons) degree in 1974.^[2][3] He then moved to England, where he studied for a Doctor of Philosophy (PhD) degree at the University of Cambridge; he was a member of Pembroke College, Cambridge.^[2] His doctoral thesis was titled "A commentary on Euboulos", and his PhD was awarded in 1979.^[4]

After completing his PhD, Hunter became a lecturer at the University of Cambridge and a Fellow of Pembroke College, Cambridge. In 2001 he was appointed as the Regius Professor of Greek at Cambridge^[5] in succession to P. E. Easterling and became a Fellow of Trinity College, Cambridge.^[6] He retired as Regius Professor in October 2021,^[2] giving his valedictory lecture on 27 September 2021.^[7]

Hunter is a member of the Academy of Athens,^[1] an Honorary Fellow of the University of Sydney^[3] and has an honorary degree from the Aristotle University of Thessaloniki.^[3] He serves on the advisory board of the periodical Materiali e discussioni per l'analisi dei testi classici.^[8] Since 2013, he is president of the council of Aristotle University of Thessaloniki.^[9]

In 2013, Hunter was elected a Fellow of the British Academy.^[10]

• Eubulus: The Fragments (Cambridge, 1983)
• A Study of Daphnis & Chloe (Cambridge, 1983)
• The New Comedy of Greece and Rome (Cambridge, 1985)
• Apollonius of Rhodes: Argonautica Book III (Cambridge, 1989)
• The 'Argonautica' of Apollonius: literary studies (Cambridge, 1993)
• Theocritus and the Archaeology of Greek Poetry (Cambridge, 1996)
• Studies in Heliodorus (Cambridge, 1998)
• Theocritus. A Selection (Cambridge, 1999)
• Theocritus: Encomium of Ptolemy Philadelphus (Berkeley, 2003)
• Plato's Symposium (Oxford, 2004)
• Tradition and Innovation in Hellenistic Poetry (with M. Fantuzzi) (Cambridge, 2004)
• The Hesiodic Catalogue of Women: Constructions and Reconstructions (Cambridge, 2005)
• The Shadow of Callimachus (Cambridge, 2006)
• On Coming After: Studies in Post-Classical Greek Literature and its Reception (Berlin, 2008)
• Wandering Poets in Ancient Greek Culture (with I. Rutherford) (Cambridge, 2009)
• Critical Moments in Classical Literature (Cambridge, 2009)
• Plutarch, How to study poetry (with D. Russell) (Cambridge, 2011)
• Plato and the Traditions of Ancient Literature: the silent stream (Cambridge, 2012)
• Hesiodic Voices. Studies in the Ancient Reception of Hesiod's Works and Days (Cambridge, 2014)
• Dionysius of Halicarnassus and Augustan Rome (ed.; with Casper C. de Jonge) (Cambridge, 2018)
• The Layers of the Text: Collected Papers on Classical Literature 2008–2021 (Berlin, 2023)

• On Coming After. Inaugural lecture as Regius Professor of Greek, 17 October 2001
• The Silence Of The Sirens: readings of Homer then and now. Lecture given at the ceremonies' hall of the University of Athens, March 2006