Climate change is affecting the distributions and growth rates of cold-blooded pest species, with dire consequences for agriculture and global food security. To address this challenge, it is essential to forecast how pests will respond to changing climates. However, current projection models typically overlook the potential for climate change adaptation. By unifying life-history theory with thermodynamics based on first principles, we here show that pest species' climate adaptation can cause substantial increases in their agricultural impact via changes in temperature-dependent resource acquisition and allocation strategies. We test these predictions by studying thermal adaptation in life-history traits and gene expression in the cosmopolitan insect pest, Callosobruchus maculatus. Five years of adaptation to simulated warming caused an almost two-fold increase in the predicted agricultural footprint of C. maculatus, while adaptation to cold temperature had little effect. Consistent with the theoretical predictions, the magnified impact under warming was driven by synergistic increases in larval resource acquisition and adult reproductive potential, resulting in a predicted double blow on agricultural yields. This suggests that adaptation in insect life-history will significantly worsen agricultural loss under future climate change and emphasizes the need for integrating a mechanistic understanding of life-history evolution into ecological forecasts of pests.