Peronospora is the largest genus of the Oomycota, responsible for causing downy mildew on a wide range of cultivated and ornamental plants worldwide. Although more than 400 Peronospora species have been described, many host-pathogen relationships have not been thoroughly explored, particularly in relation to the phylogenetic connections of pathogens from type hosts and additional hosts reported for the various described species. At the same time, infections of Peronospora on economically important hosts are an emerging threat, often with uncertainty regarding the causal agents. In this study, as an example for obligate biotrophic pathogens, 105 specimens of Peronospora parasitising species of the genus Veronica and one specimen parasitising the related host genus Paederota (both Plantaginaceae), were analysed for their morphology and phylogenetic relationships using multi-locus reconstructions. As a result, nine new Peronospora species parasitising Veronica were identified and are described in this manuscript, while the morphology of seven previously described Peronospora species was re-examined. While generally, a high degree of host specialisation was found, Peronospora verna and P. grisea were found to be indifferentiable, suggesting a recent host shift, and P. silvestris was found to also infect Globularia nudicaulis. Likewise it was found that infections on the ornamental subgenus Hebe caused by P. palustris and P. petricosa are the result of host shifts of European species onto non-native hosts. The presence of Peronospora on nearly 500 Veronica species that are not type hosts for any described Peronospora species should be re-examined, as these occurrences likely include many previously overlooked species with unknown pathogenicity.