John Thompson was born and educated in Melbourne, graduating with an arts degree from the University of Melbourne. After spending several years in England during the 1930s, he settled in Perth and joined the ABC as a broadcaster. He served in the military during World War II and continued his broadcasting career after the war. He was a correspondent for the Asian region, particularly Indonesia, and also worked for the BBC in London and South Africa. Thompson also produced many widely-admired radio documentaries and biographies.

Thompson's first book of poetry was Three Dawns Ago (1935). In total, he published four collections. His third volume, Thirty Poems (1954), won the Grace Leven Poetry Prize. Thompson conducted a series of interviews of Australian poets for Southerly and edited several anthologies, including The Penguin Book of Australian Verse (1958) with Kenneth Slessor and R. G. Howarth.

Thompson became a well-known figure in Paddington, Sydney, after campaigning against the construction of an expressway through the suburb. He died in 1968 after several operations. His funeral was attended by many people from Paddington, artists, writers, radio people and academics.

Thompson was the husband of Patricia Thompson (q.v.). Their sons are film critic Peter Thompson and actor Jack Thompson. (qq.v.)