The monarch butterfly, Danaus plexippus, is famous for its spectacular annual migration and recent worldwide dispersal.However, we know little about the genetic basis of these hallmark traits.By de novo assembling the 249-Mb monarch genome, we performed a comprehensive gene annotation on gene families likely involved in major aspects of the seasonal migration.The biological interpretation of the monarch genome advances our understanding of the genes and regulatory elements important for the long-distance migration.We then sequenced additional 101 Danaus genomes from around the globe to uncover the history of the monarchs evolutionary origin and to characterize the genes and pathways associated with migratory behavior.The results rewrite our previous understanding, showing that D.plexippus was ancestrally migratory and dispersed out of North America to occupy its broad distribution.We also find the strongest signatures of selection associated with migration is flight muscle function,resulting in more powerful flight efficiency among migratory butterflies.