In endotherms, maintenance of constant body temperature can be challenging under limited food availability. Many birds may drop body temperature below normothermia during the night to decrease energy metabolism. Such rest-phase hypothermia may also affect the level of oxidative stress due to the positive link between metabolism and reactive oxygen species. Aging may impair thermoregulatory capacity, but until today age-specific rest-phase hypothermic responses and their potential effect on oxidative stress have never been investigated. We challenged 25 zebra finches (Taeniopygia guttata) of three age groups (young, middle-aged, old) by limiting access to food for one day or provided them normal access to food. We compared body temperature through implanted data loggers and quantified oxidative stress in the morning. We found age-related differences during rest-phase hypothermia, while all three age groups remained normothermic in the night following a day with access to food. Old birds revealed the lower body temperature during night and the highest levels of oxidative damage in the following morning, while young and middle-aged birds showed higher night-time body temperature and lower values of oxidative damage. Our results lead us to propose a novel hypothesis on how aging may lead to an accumulation of oxidative damage; impairment in thermoregulatory capacity with advancing age increases the risk of oxidative stress, but only under challenging conditions. Research funded through NCN grant 2016/22/E/NZ8/00416 to ETS.