Migration is an energetically taxing phenomenon as animals move across vast, heterogenous landscapes where the cost of transport is impacted by permissible ambient conditions. In this study, we assessed the energetic demands of long-distance migration in a multigenerational ectothermic migrant, the monarch butterfly (Danaus plexippus). We tested the hypotheses that temperature-dependent physiological processes reduce energy reserves faster during migration than previously estimated, and that increasing climatic temperatures resulting from the climate crisis will intensify baseline daily energy expenditure. First, we reared monarchs under laboratory conditions to assess energy and mass conversion from fifth instar to adult stages, as a baseline for migratory adult mass and ontogenetic shifts in metabolic rate from larvae to adult. Then, using historical tag-recapture data, we estimated the movement propensity and migratory pace of fall migrants using computer simulations and subsequently calculated energy expenditure. Finally, we estimated the energy use of monarchs based on these tag-recapture data and used this information to estimate daily energy expenditure over a 57-year period. We found support for our two hypotheses, noting that incorporating standard metabolic rate into estimates of migratory energy expenditure shows higher energy demand and that daily energy expenditure has been gradually increasing over time since 1961. Our study shows the deleterious energetic consequences under current climate change trajectories and highlights the importance of incorporating energetic estimates for understanding migration by small, ectothermic migrants.