The repeated evolution of traits in organisms facing similar environmental conditions is considered to be fundamental evidence for the role of natural selection in moulding phenotypes. Yet, aside from case studies of parallel evolution and its genetic basis, the repeatability of evolution at the level of the whole genome remains poorly characterized. Here, through the use of transcriptome sequencing, we examined genomic divergence for three pairs of sister species of sunflowers. Two of the pairs (Helianthus petiolaris – H. debilis and H. annuus – H. argophyllus) have diverged along a similar latitudinal gradient and presumably experienced similar selective pressure. In contrast, a third species pair (H. exilis – H. bolanderi) diverged along a longitudinal gradient. Analyses of divergence, as measured in terms of FST, indicated little repeatability across the three pairs of species for individual genetic markers (SNPs), modest repeatability at the level of individual genes and the highest repeatability when large regions of the genome were compared. As expected, higher repeatability was observed for the two species pairs that have diverged along a similar latitudinal gradient, with genes involved in flowering time among the most divergent genes. Genes showing extreme low or high differentiation were more similar than genes showing medium levels of divergence, implying that both purifying and divergent selection contributed to repeatable patterns of divergence. The location of a gene along the chromosome also predicted divergence levels, presumably because of shared heterogeneity in both recombination and mutation rates. In conclusion, repeated genome evolution appeared to result from both similar selective pressures and shared local genomic landscapes.