The oogenesis-flight syndrome reflects the temporal allocation of energy resources between dispersal / migration and reproduction and is a key concept in research on migratory behaviour in animals. In migratory butterflies, host plant abundance and quality may act as environmental cues to switch between the two states, but the mechanisms regulating this process are virtually unknown. Here, we used an experimental set-up to assess how variation in host plant abundance affected the activity of regulatory elements in the painted lady butterfly (Vanessa cardui), a model species for insect migratory behaviour studies. Chromatin immunoprecipitation (ChIP-seq) was used to evaluate histone tail modifications of H3K27ac and H3K4me3, as a proxy for regulatory activity. The results indicate that recently eclosed females that had access to host plants invested in reproduction at an earlier stage and that variation in host plant abundance triggered significant differences in regulatory element activity via histone tail acetylation. The functions of genes in the vicinity of differentially activated regions were primarily associated with metabolism, egg shell formation, female receptivity, muscle activity, pheromone binding and chromosome maintenance. Our results provide a first glimpse into the regulatory underpinnings of how females perceive the environment and allocate resources for either migration or reproduction and a starting point for more detailed understanding of the links between environmental variation, gene regulation and behaviour in butterflies.