The monarch butterfly , Danaus plexippus , is famous for its spectacular annual migration across North America , recent worldwide dispersal, and orange warning colouration . Despite decades of study and broad public interest , we know little about the genetic basis of these hallmark traits . Here we uncover the history of the monarch’s evolutionary origin and global dispersal , characterize the genes and pathways associated with migratory behaviour , and identify the discrete genetic basis of warning colouration by sequencing 101 Danaus genomes from around the globe . The results rewrite our understanding of this classic system , showing that D. plexippus was ancestrally migratory and dispersed out of North America to occupy its broad distribution . We find the strongest signatures of selection associated with migration centre on flight muscle function , resulting in greater flight efficiency among migratory monarchs , and that variation in monarch warning colouration is controlled by a single myosin gene not previously implicated in insect pigmentation .