1. The ability to cope with heatwaves is likely to influence species success amidst climate change. However, relatively little is known about heat-coping mechanisms in endotherms, which are increasingly pushed to their thermoregulatory limits. We experimentally elevated nest temperatures by 4.5°C for 4 hours, focused on 12-day-old tree swallows (Tachycineta bicolor). 2. Nestlings exposed to sub-lethal heat moved towards cooler air at the nest box entrance, they panted more, and they weighed less than controls, suggesting panting-induced water loss. They also exhibited higher heat shock protein (HSP) gene expression in the blood, alongside widespread transcriptional differences related to antioxidant defenses, inflammation, and apoptosis. Nestlings exposed to milder heat were more likely to recruit into the breeding population, suggesting these coping mechanisms may be quite effective. 3. We also tested hypotheses on the drivers of variation in HSP gene expression, which was especially marked after heat-exposure. Even siblings in the same nest differed in HSP gene expression by over 14-fold. Heat-induced HSP levels were unrelated to individual body mass, or among-nest differences in brood size, temperature, and behavioral thermoregulation. However, nest ID explained a significant amount of HSP variation, which was larger between nests than within nests, pointing to genetic or early developmental factors 4. These results fill key knowledge gaps on thermoregulatory mechanisms in birds. We document ample individual variation upon which selection may act in the context of climate change and we underscore the need to understand intra-specific variation, an oft-ignored element that nevertheless shapes what is possible for future adaptation or acclimation to heat.