Hunter was born in Rothesay on the Isle of Bute. His family emigrated to California in 1892 and by the turn of the century he was making a living there as an illustrator. Little is known of Hunter's early work as much of it was destroyed in the San Francisco earthquake of 1906. He moved to Glasgow soon afterwards. During the 1920s Hunter emerged alongside Cadell, Fergusson and Peploe as one of a group of artists who became known as 'Scottish Colourists'. They were all influenced, in varying degrees, by the pure, bright colour and loose brushwork of French Impressionsim, Post-Impressionism and fauve painting.