The rapid rate of climate change will impose tremendous stress on biodiversity. Most ecologists expect the poleward edge of a species’ range to expand as marginal conditions improve under warming, but peripheral populations may be adapted to local conditions.  Traits that limit dispersal and increase exposure to selective agents can lead to the emergence of genetic differences among populations, differences that confer local fitness advantages.  These local differences may be critical under climate change because peripheral populations may be perturbed from local fitness optima, posing a threat of population contraction or extinction.  We explore this evolutionary constraint on the ecological response of species to climate change by comparing adaptive and genetic differences in two butterfly species with contrasting ecological traits.  To test for local adaptation between populations within each species, we performed reciprocal translocation experiments using individuals from central and peripheral locales, and we analyzed the genetic structure within their range using microsatellite markers. We find pronounced evidence for greater adaptation to peripheral conditions in the small, specialist and support that observation with molecular data, which indicate higher levels of population differentiation in the northern part of the species range with more restricted gene flow.  In contrast, we see poor performance under peripheral conditions in the large, generalist and genetic admixture throughout its range facilitated by higher levels of gene flow. Thus, the potential for peripheral adaptation to affect poleward colonization suggests that ecologists should consider evolutionary constraints on the opportunity for range shifts under global warming.