Because of the strong morphological similarity of the powdery mildew fungi that infect papaveraceous hosts, a total of 39 samples were studied to reveal the phylogeny and host range of these fungi. ITS and 28S sequence analyses revealed that the isolates identified earlier as Erysiphe cruciferarum on papaveraceous hosts represent distinct lineages and differ from that of E. cruciferarum sensu stricto on brassicaceous hosts. The taxonomic status of the anamorph infecting Eschscholzia californica was revised, and therefore, a new species name, Erysiphe eschscholziae, is proposed. The taxonomic position of the Pseudoidium anamorphs infecting Glaucium flavum, Meconopsis cambrica, Papaver dubium, and Stylophorum diphyllum remain unclear. This study revealed that Erysiphe macleayae exhibits a specific host range different from that of E. cruciferarum, the common pathogen of papaveraceous hosts. Although E. macleayae occurred naturally on Macleaya cordata, Macleaya microcarpa, M. cambrica, and Chelidonium majus only, our inoculation tests revealed that the fungus was capable of infecting Argemone grandiflora, Glaucium corniculatum, Papaver rhoeas, and Papaver somniferum, indicating that these plant species may also be taken into account as potential hosts. Erysiphe cruciferarum originating from P. somniferum was not able to infect A. grandiflora, C. majus, E. californica, M. cordata, and P. rhoeas. The emergence of E. macleayae on M. microcarpa is reported here for the first time from the Czech Republic and Slovakia. The appearance of chasmothecia of E. macleayae on C. majus in Slovakia was reported, as well. Erysiphe cruciferarum was identified on G. corniculatum and reported here for the first time from Slovakia.