Many insects exhibit geographical variation in voltinism, the number of generations produced per year. This includes high‐latitude species in previously glaciated areas, meaning that divergent selection on life cycle traits has taken place during or shortly after recent colonization. Here, we use a population genomics approach to compare a set of nine Scandinavian populations of the butterfly Pararge aegeria that differ in life cycle traits (diapause thresholds and voltinism) along both north–south and east–west clines. Using a de novo‐assembled genome, we reconstruct colonization histories and demographic relationships. Based on the inferred population structure, we then scan the genome for candidate loci showing signs of divergent selection potentially associated with population differences in life cycle traits. The identified candidate genes include a number of components of the insect circadian clock (timeless, timeless2, period, cryptochrome and clockwork orange). Most notably, the gene timeless, which has previously been experimentally linked to life cycle regulation in P. aegeria, is here found to contain a novel 97‐amino acid deletion unique to, and fixed in, a single population. These results add to a growing body of research framing circadian gene variation as a potential mechanism for generating local adaptation of life cycles.