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Most studies of climate change impacts focus on the effects of summer temperatures, which can immediately impact fitness of breeders, but winter temperatures are expected to have a greater impact on development and growth of animals with long-lasting consequences. Exposure to warmer temperatures can increase cellular oxidative damage in ectotherms. Yet, it is unknown whether thermal stress during early life has prolonged effects on oxidative status during adulthood. In an experiment using F1 fish originated from a wild three-spined stickleback population at the southern edge of its European distribution, we examined whether experimental thermal conditions experienced in winter had carry-over effects on oxidative status and telomere length, a marker of accumulated stress, in the soma and germline during adulthood. For this, oxidative DNA damage, enzymatic antioxidant activities and telomere length were measured three months after the termination of the temperature manipulation. In addition, we tested whether such delayed effects, if any, were due to individuals' compensatory growth after experiencing unfavourable growth conditions in winter. Warm acclimation during winter induced increased levels of oxidative DNA damage in muscle and sperm and increased enzymatic antioxidant defences in muscle during the breeding season. Telomere length of adult fish was not influenced by thermal conditions experienced during early life. Winter temperature manipulation influenced fish to alter the temporal pattern of growth trajectories across the juvenile and adult stages. Fish reared in warm winter conditions grew at a slower rate than the controls during the period of temperature manipulation then accelerated body mass gain to catch up during the breeding season. Faster somatic growth during the breeding season incurred a higher cost in terms of oxidative damage in the warm-treated individuals. For the first time, we experimentally show the long-lasting detrimental effects of thermal stress on and the positive link between catch-up growth and oxidative DNA damage in the soma and germline. Winter temperature increases due to climate change can reduce fertility and survival of fish by inducing catch-up growth. The detrimental effects of winter climate change may accumulate across generations through the pre-mutagenic DNA damage in the germline.