Colour pattern has served as an important phenotype in understanding the process of natural selection, particularly in brightly coloured and variable species like butterflies. However, different selective forces operate on aspects of colour pattern, for example by favouring warning colours in eyespots or alternatively favoring investment in thermoregulatory properties of melanin. Additionally, genetic drift influences colour phenotypes, especially in populations undergoing population size change. Here, we investigated the relative roles of genetic drift and ecological selection in generating the phenotypic diversity of the butterfly Parnassius clodius. Genome‐wide patterns of single nucleotide polymorphism data show that P. clodius forms three population clusters, which experienced a period of population expansion following the last glacial maximum and have since remained relatively stable in size. After correcting for relatedness, morphological variation is best explained by climatic predictor variables, suggesting ecological selection generates trait variability. Solar radiation and precipitation are both negatively correlated with increasing total melanin in both sexes, supporting a thermoregulatory function of melanin. Similarly, wing size traits are significantly larger in warmer habitats for both sexes, supporting a Converse Bergmann Rule pattern. Bright red coloration is negatively correlated with temperature seasonality and solar radiation in males, and weakly associated with insectivorous avian predators in univariate models, providing mixed evidence that selection is linked to warning coloration and predator avoidance. Together, these results suggest that elements of butterfly wing phenotypes respond independently to different sources of selection and that thermoregulation is an important driver of phenotypic differentiation in Parnassian butterflies.