SummaryThe physiological and ecological impact of the thermal environment across life stages can result in trade‐offs that determine fitness and population dynamics. Understanding mechanisms and consequences of local adaptation for any organism that overwinters requires taking a cross‐seasonal perspective.We used a trait‐based approach to distinguish variation among ecotypes in ecological and physiological responses to overwintering conditions. We used fall webworms (Hyphantria cunea;Lepidoptera:Arctiidae) fromOttawa,Ontario andColumbusOhio, representing the centre and periphery of the native range.We hypothesized that populations would be locally adapted to their overwintering environments, with fitness maximized under natal overwintering conditions. We predicted that this local adaptation would result from modulation of rates of energy use, growth and development.Each ecotype had higher overwinter survival in their natal compared with non‐natal winter environment, and this was associated with larger pupal mass, size and carbohydrate reserves at the end of winter. This suggests that the ecotypes are locally adapted to winter conditions. Larger adults laid more eggs, but there was no effect of ecotype or environment on fecundity.Pupae overwintering at warm, energetically demanding, southern temperatures suppressed metabolic rates in autumn, and developed more quickly in the spring, compensating for energetic demands of warmer winters. Northern ecotypes had lower thermal sensitivity of metabolism, leading to higher metabolic rates at cool temperatures that correlated with faster post‐winter development.Local adaptation to winter conditions suggests performance of peripheral populations may not be enhanced by warming winters. Decoupling of winter and growing season temperatures may negatively impact ectotherms.