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Abstract In temperate regions, temperature and photoperiod are considered the main drivers of life‐history and metabolic variation in ectotherms. Yet, while crucially important to understand responses to global warming, how responses to temperature depend on natural variation in photoperiod is not fully understood. Here, we investigated the effects of naturally varying temperatures under two different photoperiod regimes on life‐history, morphological and physiological traits in the damselfly Lestes sponsa . We raised larvae in incubators under four treatments: weekly changing early or late photoperiod with weekly changing ambient or warming +5°C temperature. When larvae reached the prefinal instar, they were phenotyped for development and size‐related traits and processed for physiological analyses related to energy, immune system (phenoloxidase activity) and oxidative stress. For the life‐history traits, our results revealed clear differences between treatments with individuals under the late photoperiod developing faster at the cost of being smaller, consistent with the higher perceived time constraints. Temperature explained a smaller proportion of phenotypic variance in individuals raised under the late than early photoperiod, especially for development time and mass, indicating less thermal plasticity under time constraints. For the physiological traits, differences between treatments were smaller with lower levels of energy consumed and phenoloxidase activity under the late than the early photoperiod. Temperature explained a greater proportion of physiological variance on individuals raised under the late photoperiod. The observed covariation between development time and physiological traits suggests a coupling between both types of traits and some costs associated with fast development in the late photoperiod in terms of reduced immune system activity and more oxidative damage to lipids. Our results support the general prediction that seasonal variation in the photoperiod is an important environmental cue shaping life‐history traits in ectotherms living in temperate regions, which moreover may shape warming response.s