Howkins' media career spans TV, film, digital media, publishing and consulting with companies including HandMade plc, Hotbed Media, HBO and, from 1982 to 1996, Time Warner. He is a former chairman of the London Film School and is a former Executive Director of the International Institute of Communications, an independent, non-profit membership organization that focusses on critical policy and regulatory issues in the telecom and media.
In 2006 he became chairman of the John Howkins Research Centre on the Creative Economy, launched by the Shanghai Municipal Government at the Shanghai School of Creativity, Shanghai Theatre Academy. He is an adviser to the Shanghai Creative Industries Association and the Shanghai Creative Industry Centre. Since 2007 he has chaired BOP Consulting, an independent research and strategy consultancy who maximise the potential of culture, media and creativity, in parallel with his independent consulting work.