John Preston attended Marlborough College in Wiltshire from 1967 to 1971. He worked as the Arts Editor of The Evening Standard and The Sunday Telegraph. He was The Sunday Telegraph's television critic for ten years and one of its chief feature writers.

Preston wrote four novels between 1996 and 2007. All are set in England in the recent past: Ghosting in the world of radio and television in the 1950s; Ink in the dying days of Fleet Street's importance in journalism in the 1980s; Kings of the Roundhouse in strife-torn London in the 1970s; and The Dig in the 1930s. Preston wrote The Dig, a novelised account of the Sutton Hoo archaeological dig, after discovering that his aunt had been one of the key participants. The Dig has been made into a feature film starring Ralph Fiennes, Carey Mulligan, and Lily James, released on Netflix in 2021.

A Very English Scandal, Preston's non-fiction account of the Jeremy Thorpe affair of the 1970s, was adapted into a television miniseries starring Hugh Grant and Ben Whishaw in 2018. His 2020 non-fiction book, Fall: The Mystery of Robert Maxwell, won the Costa Book Award for biographies in 2021, and is being adapted for television by Working Title.