Many small animals routinely regulate resting body temperature several degrees below active-phase levels (rest-phase hypothermia), which reduces heat transfer rate and tissue oxygen demand and so may confer energy savings. Small birds that winter at high latitude show limited capacity for rest-phase hypothermia, meaning they cannot avoid upregulating heat production when facing winter cold. Substrates for upholding body temperature are provided by mitochondria in the form of adenosine triphosphate (ATP), but mitochondrial respiration is probably lower during hypothermia because of the temperature-dependence of biological processes (i.e., Q10 effect). Thus, there could be a conflict between increased organismal fuel demand and a lower mitochondrial capacity to provide it during rest-phase hypothermia. We studied this enigma by assessing mitochondrial function in the blood cells of wintering great tits (Parus major) that had spent the preceding night in warm, mild, or cold temperatures, at each of a hypothermic and a normothermic thermal state in vitro. Hypothermia reduced mitochondrial respiration by 13 %. However, this did not affect respiration allocated to oxidative phosphorylation, because hypothermia was also associated with a reduction in non-phosphorylating respiration, from 17 % in normothermia to 4 % in hypothermia. The proportion of non-phosphorylating respiration also decreased in response to colder night temperatures Thus, the coupling efficiency between electron transport and ATP production in maximally stimulated cells increased from 91% in normothermia to 98% in hypothermia. Our study shows that mitochondrial function can be highly plastic on short temporal scales. Thus, functional changes in the electron transport system might safeguard ATP production at lower tissue temperatures and when organismal demand for fuel increases in cold winter temperatures.