Dispersal capacity is a key life history trait especially in species inhabiting fragmented landscapes. Evolutionary models predict that, given sufficient heritable variation, dispersal rate responds to natural selection imposed by habitat loss and fragmentation. Here, we estimate phenotypic variance components and heritability of flight and resting metabolic rates in an ecological model species, the Glanville fritillary butterfly, in which flight metabolic rate is known to correlate strongly with dispersal rate. We modeled a two-generation pedigree with the animal model to distinguish additive genetic variance from maternal and common environmental effects. The results show that flight metabolic rate is significantly heritable, with additive genetic variance accounting for about 40% of total phenotypic variance; thus flight metabolic rate has the potential to respond to selection on dispersal capacity. Maternal influences on flight metabolism were negligible. Heritability of flight metabolism was context-dependent, as in stressful thermal conditions environmentally induced variation dominated over additive genetic effects. There was no heritability in resting metabolic rate, which was instead strongly influenced by maternal effects. This study contributes to a mechanistic understanding of the evolution of dispersal-related traits, a pressing question in view of the challenges posed to many species by changing climate and fragmentation of natural habitats.