Extreme heatwaves threaten global biodiversity, yet the sublethal carry-over effects of developmental thermal stress on adult fitness remain poorly understood. We addressed this knowledge gap for bumblebees, key pollinators that face alarming population declines, using a controlled in vitro approach. We exposed Bombus terrestris pupae to cyclic thermal stress to evaluate emergence success, adult longevity, and morphological traits. Cyclic thermal stress caused significant acute pupal mortality (up to 30% reduced emergence) and, crucially, deferred mortality, significantly reducing adult longevity (hazard ratio, HR = 2.00) in both workers and males. Rearing in vitro at 34°C showed no significant difference compared to individuals that developed naturally in their natal colony (HR = 0.95). Antennal and wing deformations served as powerful hazard indicators (HR = 2.38) for premature adult mortality. Our findings reveal that cyclic thermal stress during pupal development imposes irreversible developmental damage, undermining adult physiological resilience.