Hypericum perforatum (St. John’s wort) is a widespread Eurasian perennial plant species with remarkable variation in its morphology, ploidy and breeding system. Koch et al. analyse extensive field collections and demonstrate that H. perforatum is not of hybrid origin, and for the first time document wild diploid populations. They find various cryptic gene pools and demonstrate past and contemporary gene flow within and between gene pools, and with the sister species H. maculatum. Cytogenetic analyses highlight that these processes are highly influenced by the reproductive system in both species, with a switch to predominantly apomictic reproduction in polyploids, irrespective of their evolutionary origin.