From the 1935 general election until his death, he was Member of Parliament (MP) for the Bodmin constituency in Cornwall. After his death, his American-born wife Beatrice was elected unopposed to succeed him as MP.
He served as Parliamentary Secretary to the Ministry of Supply from July to September 1939, when World War II broke out. A flight lieutenant and fighter pilot with the Royal Air Force, he was killed shortly after the Battle of Britain. He was buried at Schoonselhof cemetery, Antwerp, Belgium.
Rathbone was the nephew of Eleanor Rathbone, who had been an independent MP for the Combined English Universities between 1929 and 1946, and a staunch women's rights campaigner. He was a grandson of William Rathbone, Liberal MP for Liverpool and later Carnarvonshire.
- Hansard 1803–2005: contributions in Parliament by John Rathbone
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