Michael Thwaites was born in Brisbane and educated at Ivanhoe Grammar School, Melbourne, and Geelong Grammar School. He entered the University of Melbourne in 1934, graduating with a first-class degree in classics. In 1937 he was awarded a Rhodes Scholarship to Oxford where he won the Newdigate prize for his poem 'Milton Blind'. He was also the first Australian to be awarded the King's Medal for Poetry. During World War II, he served in the Royal Naval Volunteer Reserve 1939-1945. A series of war poems were included in his first volume, Jervis Bay and Other Poems (1943) and he also wrote an account of these years in Atlantic Odyssey (1999).
Returning to Australia in 1947, Thwaites lectured in English for two years at the University of Melbourne before being recruited by ASIO to head the agency's counter-espionage operations. He remained with ASIO until 1971 and was a central figure in the defection of Vladimir and Evdokia Petrov in 1954. The Petrov's lived with Thwaites in a safe house and he helped them to write a book on the affair, Empire of Fear (1956). In 1971 Thwaites retired from ASIO and was appointed deputy head of the Parliamentary Library, a position he held for the next five years. His own account of the Petrov Affair, Truth Will Out was published in 1980.
In addition to the publication of Milton Blind (1938), Thwaites published four volumes of poetry, including Unfinished Journey: Collected Poems (2004). According to the Oxford Companion to Australian Literature, Thwaites' poetry is 'traditional in rhetoric and theme, [reflecting] his commitment to the Moral Rearmament movement and his admiration for such poets as John Masefield.'