The demands of long-distance flight represent an important evolutionary force operating on the traits of migratory species. Monarchs are widespread butterflies known for their annual migrations in North America. We examined divergence in wing morphology among migratory monarchs from eastern and western N. America, and nonmigratory monarchs in S. Florida, Puerto Rico, Costa Rica, and Hawaii. For the three N. American populations, we also examined monarchs reared in four common environment experiments. We used image analysis to measure multiple traits including forewing area and aspect ratio; for laboratory-reared monarchs we also quantified body area and wing loading. Results showed wild monarchs from all nonmigratory populations were smaller than those from migratory populations. Wild and captive-reared eastern monarchs had the largest and most elongated forewings, whereas monarchs from Puerto Rico and Costa Rica had the smallest and roundest forewings. Eastern monarchs also had the largest bodies and high measures of wing loading, whereas western and S. Florida monarchs had less elongated forewings and smaller bodies. Among captive-reared butterflies, family-level effects provided evidence that genetic factors contributed to variation in wing traits. Collectively, these results support evolutionary responses to long-distance flight in monarchs, with implications for the conservation of phenotypically distinct wild populations.