Evidence from a number of species suggests that behaviours associated with social rank are positively correlated with metabolic rate. These studies, however, are based on metabolic measurements of isolated individuals, thereby ignoring potential effects of social interactions on metabolic rates. Here, we characterised three pertinent metabolic indices in the two predominant genetic colour morphs of the Gouldian finch (Erythrura gouldiae): diurnal resting metabolic rate (RMR), nocturnal basal metabolic rate (BMR) and exercise-induced maximal metabolic rate (MMR). Research reveals that red-headed morphs consistently dominate the less aggressive black-headed morphs and that the two morphs differ in other behavioural and physiological traits. We measured daytime RMR of intermorph naïve birds (first-year virgin males maintained in total isolation from opposite colour morphs) and their metabolic responses to viewing a socially unfamiliar bird of each colour. Subsequently, each bird was placed in a home cage with an opposite colour morph (intermorph exposed) and the series of measurements was repeated. Daytime RMR was indistinguishable between the two morphs, regardless of whether they were intermorph naïve or intermorph exposed. However, both red- and black-headed birds showed a greater short-term increase in metabolic rate when viewing an unfamiliar red-headed bird than when seeing a black-headed bird, but only when intermorph naïve. Measurements of BMR and exercise-induced MMR did not differ between the two morphs, and consequently, aerobic scope was indistinguishable between them. We propose that the behavioural differences between these two sympatric morphs are functionally complementary and represent evolutionary stable strategies permitting establishment of dominance status in the absence of metabolic costs.