In many migratory insects, migration occurs during the prereproductive phase of the life cycle. This trait probably arises from a trade-off between migration and reproduction and in females has been termed the ‘oogenesis–flight syndrome’. However, the generality of this syndrome has been questioned, especially for monomorphic insects. We studied the relationship between migration and reproduction in the highly cosmopolitan painted lady butterfly, Vanessa cardui, which in the Palaearctic undertakes the longest known multigenerational migration circuit of any insect. We tested for the oogenesis–flight syndrome in both spring and autumn migrants in two regions linked by migration, North Africa and northern Spain. Field observations were combined with laboratory experiments to determine the life span and the age at first mating to unravel the reproductive strategy observed in wild-caught individuals. Females and males wait on average around 5–6 days before mating, and field data revealed that mating frequencies increased rapidly once females reached a medium wing wear category. There were seasonal differences in mating frequencies in the study regions depending on whether the region acted as a source or as a destination for migrants, and in the latter case there were almost twice as many mated females. Moreover, a great majority of females collected during migratory flights were unmated, the remaining females having mated only very recently. Our results thus strongly indicate that the painted lady fulfils the oogenesis–flight syndrome, as migration is concentrated in its relatively short prereproductive period. Field data also showed a high positive correlation between mating frequency and host plant abundance, which suggests that mated females are able to locate potential breeding areas. This, together with the high fecundity estimated in laboratory trials, makes the painted lady a highly successful migratory insect.