The evolution of adaptive phenotypic plasticity, whereby organisms respond to cues to produce phenotypes appropriate to their future environment, is not well understood. Male orange-tip Anthocharis cardamines butterflies utilizing the host-plant lady's smock Cardamine pratensis (on which food is limiting) are smaller and emerge earlier than those utilizing garlic mustard Alliaria petiolata. Since small size reduces dispersal rate, this coupling produces an adaptive ‘emerge early and wait' mate location strategy. Here we show that early emergence is abolished when males are subjected to a severely restricted diet, which we take to be the ancestral response. We propose that the derived (early emergence) response on C. pratensis has evolved through sex-specific changes in the timing and efficiency of developmental and metabolic processes in late larval life. Our results offer broad support to the idea that adaptive phenotypic plasticity can evolve through the selection of cue-sensitive modifier genes controlling initially passive plastic responses.