Nonhost resistance is hypothesized to protect plants in a nonspecific manner. For highly specialized parasites, this hypothesis applies not only to distantly related plants but also to resistant congeners of the host species. Congeners of Populus spp. were hybridized to create two interspecific hybrid poplar pedigrees (i.e., Populus trichocarpa × P. deltoides and P. trichocarpa × P. maximowiczii). The pedigrees were planted in a randomized, replicated “common garden” on Vancouver Island so that they were exposed to parasites of the native P. trichocarpa. Monogenic and oligogenic resistance to two ascomycetous, parasitic fungi (i.e., Venturia inopina and a Taphrina sp.) segregated in a parasite-specific manner in each pedigree. However, these resistance genes were not inherited from the native host, P. trichocarpa. Instead, resistance was inherited from the allopatric, nonhost congeners, P. deltoides (eastern cottonwood) and P. maximowiczii (Japanese poplar). Thus, we found that major genes condition parasite-specific, nonhost resistance, as has been true in earlier studies of this kind with additional parasites of Populus spp. The selective force responsible for evolutionary maintenance of such genes is unknown.