As photoperiod shortens with the approach of winter, small mammals should reduce their energy expenditure to survive periods of food limitation. However, within seasons, animals should balance their energy budgets as abiotic conditions change, sometimes unpredictably; cold spells should increase heat production, while warm spells should do the opposite. Therefore, we addressed specific questions about the possible interactions between seasonal acclimatization and the intra-seasonal phenotypic flexibility of metabolic rate. We hypothesized that phenotypic flexibility in small mammals differs seasonally and is greater in summer than in winter, and predicted that seasonal adjustments in energetics, which are driven by photoperiod, overwhelm the influence of variations in the thermal environment. We measured body mass, basal metabolic rate (BMR), facultative non-shivering thermogenesis (fNST), body temperature, and calculated minimum thermal conductance in Siberian hamsters Phodopus sungorus. Animals were acclimated to winter-like, and then to summer-like conditions and, within each season, were exposed twice, for 3 weeks to 10, 20 or 28 °C. We used differences between values measured after these short acclimation periods as a measure of the scope of phenotypic flexibility. After winter acclimation, hamsters were lighter, had lower whole animal BMR, higher fNST than in summer, and developed heterothermy. After these short acclimations to the above-mentioned temperatures, hamsters showed reversible changes in BMR and fNST; however, these traits were less flexible in winter than in summer. We conclude that seasonal acclimation affects hamster responses to intra-seasonal variations in the thermal environment. We argue that understanding seasonal changes in phenotypic flexibility is crucial for predicting the biological consequences of global climate changes.Electronic supplementary materialThe online version of this article (doi:10.1007/s00360-016-0959-3) contains supplementary material, which is available to authorized users.