From 1972 to 1975, he studied English at Jesus College, Cambridge, United Kingdom, where he founded, with Charlie Bulbeck and Charles Lambert, the Blue Room, a society devoted to the propagation of poetry and the other fine arts.

His first publication, Of Western Limit (a collaboration with Charles Lambert), appeared in 1974, the year in which Wilkinson won the Chancellor's Medal for Poetry.

His most recent collections are Reckitt's Blue (2013), Down to Earth (2008), Lake Shore Drive (2006), Contrivances (2003) and Effigies against the Light (2001); a chapbook titled Iphigenia appeared in 2004, and his 1986 collection, Proud Flesh, was re-issued in 2005 with an introduction by Drew Milne.

John Wilkinson has held a Frank Knox Fellowship at Harvard University, and was a Fulbright Distinguished Scholar in 2003/04 at the Nathan S. Kline Institute.

From 2005 to 2010 he was Writer in Residence and thereafter Research Professor in the Department of English at the University of Notre Dame.