He began teaching in 1962 at the State University of New York, then continued at the University of Manchester. From 1966 to 2002 he was a Fellow and tutor of Magdalen College, Oxford; he is now Fellow Emeritus.
Fuller has published 15 collections of poetry, including Stones and Fires (1996), Now and for a Time (2002), Song and Dance (2008) and the recent The Dice Cup (2014). Chatto and Windus published a Collected Poems in 1996. His novel Flying to Nowhere (1983), a historical fantasy, won the Whitbread First Novel Award, and was nominated for the Booker Prize. In 1996 he won the Forward Prize for Stones and Fires and in 2006 the Michael Braude Award for Light Verse. He has also written collections of short stories and several books for children. His poem Ship of Sounds, illustrated with a wood engraving by the artist Garrick Palmer, was published in 1981 in an edition of 130 by The Gruffyground Press.
In 1968, John Fuller established the Sycamore Press, which he ran from his garage. The Sycamore Press published some of the most influential and critically acclaimed poets of the latter half of the twentieth century, such as W. H. Auden, Philip Larkin and Peter Porter. In addition to these established authors, the Press sought to promote younger poets, many of whom have gone on to achieve great success. The Sycamore Press ceased operations in 1992, and is an excellent example of a British small press, publishing for motives other than profit. John Fuller and the Sycamore Press (Bodleian Library, 2010) includes an interview with John Fuller and personal reflections by Sycamore Press authors about Fuller, the press and the works it produced. The book also includes a bibliography of the pamphlets and broadsides Fuller produced.
Fuller is a Fellow of the Royal Society of Literature.