Theory indicates that spatial scale and habitat configuration are fundamental for coevolutionary dynamics and how diversity is maintained in host–pathogen interactions. Yet, we lack empirical data to translate the theory to natural host–parasite systems. In this study, we conduct a multiscale cross-inoculation study using the specialist wild plant pathogen Podosphaera plantaginis on its host plant Plantago lanceolata. We apply the same sampling scheme to a region with highly fragmented (Åland) and continuous (Saaremaa) host populations. Although theory predicts higher parasite virulence in continuous regions, we did not detect differences in traits conferring virulence among the regions. Patterns of adaptation were highly scale dependent. We detected parasite maladaptation among regions, and among populations separated by intermediate distances (6.0–40.0 km) within the fragmented region. In contrast, parasite performance did not vary significantly according to host origin in the continuous landscape. For both regions, differentiation among populations was much larger for genetic variation than for phenotypic variation, indicating balancing selection maintaining phenotypic variation within populations. Our findings illustrate the critical role of spatial scale and habitat configuration in driving host–parasite coevolution. The absence of more aggressive strains in the continuous landscape, in contrast to theoretical predictions, has major implications for long-term decision making in conservation, agriculture, and public health.