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ABSTRACT Many terrestrial ectotherms have gone to great evolutionary lengths to adapt to long cold winters; some have even evolved the ability to tolerate the freezing of most of the extracellular fluid in the body. Now, however, high‐elevation and high‐latitude winters are experiencing an accelerated period of warming. Specialised winter adaptations that promoted fitness in a seasonally frozen environment may soon be superfluous or even maladaptive. We ask whether winter adaptations include changes in immune functions, and whether changing winter conditions could exert disparate effects on populations of a wide‐ranging terrestrial ectotherm, the wood frog (Lithobates sylvaticus). By rearing wood frogs from ancestral winter environments that vary in length and temperature in a common garden, and reciprocally exposing post‐metamorphic frogs to unfrozen and frozen artificial winter conditions in the lab, we were able to decompose transcriptomic differences in ventral skin gene expression into those that were environmentally induced (responsive to temperature) and genetically determined and those that varied as an interaction between the genotype and environment. We found that frogs from harsh ancestral winter environments constitutively upregulated immune processes, including cellular immunity, inflammatory processes and adaptive immune processes, as compared to frogs from mild ancestral winter environments. Further, we saw that the expression of several genes varied in an interaction between the genotype and artificial winter. We suggest that just as winter climates likely served as the selective force resulting in remarkable winter adaptations such as freeze tolerance, they may have also induced constitutive changes in immune gene expression.