Jack Lindsay was born in Melbourne, the son of Norman Lindsay (q.v.). The family moved to Sydney in 1901 when Norman was appointed as a cartoonist on the Bulletin. He later moved to Brisbane with his mother in 1909 when his parents separated. After an irregular schooling before the age of twelve, he attended the Brisbane Grammar School and graduated with first class honours from the University of Queensland in 1921. He moved back to Sydney in June 1921 and participated actively in the literary scene, founding the magazine Vision, co-editing the anthology Poetry in Australia 1923 and co-founded the Fanfrolico Press with John Kirtley (q.v.). In 1926 he and Kirtley took the press to England. Lindsay never returned to Australia, leaving his wife, Janet Beaton (q.v.), and an Australian literary career that had produced much literary journalism and several volumes of poetry.
After the Fanfrolico Press folded at the end of 1930, Lindsay began to write historical novels, political commentary and literary biographies. Between 1934 and 1941 he wrote more then thirty books, but did not achieve great popularity. His interest in the Nietzschean vision of his famous father was replaced by an interest in Marxism which inspired much of his later fiction and non-fiction, earning him the Soviet Badge of Honour in 1968. After serving in World War II, during which he worked as a script writer for the War Office, Lindsay continued his prolific writing career. Over the next three decades he wrote poetry, drama, histories, translations, biographies, novels, criticism and more, bringing his total number of books to more than 150. In addition to his early poetry and criticism, Lindsay's most significant work with Australian content are his three volumes of autobiography which demonstrate a continued identification with his birth country.
Lindsay received a number of awards an honours, including a D. Litt from the University of Queensland (1968) and an AM (1981); in 1980 he was elected as a life member of the Association for the Study of Australian Literature. In 1985 Lindsay moved to Cambridge with Meta Waterdrinker, his companion of more than thirty years and mother of his two children. He died there five years later.