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Summary Animal eyes are some of the most widely recognisable structures in nature. Due to their salience to predators and prey, most research has focused on how animals hide or camouflage their eyes [1]. However, across all vertebrate Classes, many species actually express brightly coloured or conspicuous eyes, suggesting they may have also evolved a signalling function. Nevertheless, perhaps due to the difficulty with experimentally manipulating eye appearance, very few species beyond humans [2] have been experimentally shown to use eyes as signals [3]. Using staged behavioural trials we show that Trinidadian guppies ( Poecilia reticulata ), which can rapidly change their iris colour, predominantly express conspicuous eye colouration when performing aggressive behaviours towards smaller conspecifics. Furthermore, using a novel, visually realistic robotic system to create a mismatch between signal and relative competitive ability, we show that eye colour is used to honestly signal aggressive motivation. Specifically, robotic ‘cheats' (that is, smaller, less-competitive robotic fish that display aggressive eye colouration when defending a food patch) attracted greater food competition from larger real fish. Our study suggests that eye colour may be an under-appreciated aspect of signalling in animals, shows the utility of our biomimetic robotic system for investigating animal behaviour, and provides experimental evidence that socially mediated costs towards low-quality individuals may maintain the honesty of dynamic colour signals.