Theory predicts that phenotypic flexibility will evolve in variable yet predictable environments. What is less well understood is how the relative degree of flexibility in flexible traits might relate to the environment, however. It has been proposed that the degree of flexibility exhibited by an individual will positively correlate with the environmental heterogeneity it experiences, yet there are few empirical examples to support this. To help uncover the mechanisms driving geographic variation in physiological flexibility, we integrated assays of population genetic variation with whole-organism measures of thermogenic performance and indices of environmental heterogeneity for individuals in the songbird genus Junco . Juncos inhabit a wide range of environments from montane forests of Central America to the taiga of northern Alaska, offering an opportunity to understand how environmental conditions may drive patterns in flexibility across this diverse group. We combined measures of thermogenic capacity for 292 individuals collected across the United States, 28,000 single nucleotide polymorphisms genotyped in 192 individuals, and laboratory acclimation experiments replicated on five Junco populations. Across their range, juncos: (1) differed in their thermal performance responses to temperature variation in situ ; (2) exhibit variation in their degree of thermogenic flexibility that correlates with the heterogeneity of their native thermal environment; and (3) harbor genetic variation that also correlates with temperature heterogeneity. Together, these results support theoretical predictions and suggest that thermogenic flexibility may play a key role in local adaptation in this broadly distributed lineage.