Crop pathogens reduce yield and contribute to global malnourishment. Surveillance not only detects presence/absence but also reveals genetic diversity, which can inform our understanding of rapid adaptation and control measures. An often neglected aspect is that pathogens may also use crop wild relatives as alternative hosts. This study develops the beet (Beta vulgaris) rust (Uromyces beticola) system to explore how crop pathogens evolve to evade resistance using a wild reservoir. We test predictions that crop selection will drive virulence gene differentiation and affect rates of sex between crop- and wild-host rust populations. We sequenced, assembled, and annotated the 588 Mb beet rust genome, developed a novel leaf peel pathogen DNA extraction protocol, and analysed genetic diversity in 42 wild and crop isolates. We found evidence for two populations: one containing exclusively wild-host isolates; the other containing all crop-host isolates, plus five wild isolates. Effectors showed greater diversity in the exclusively wild population and greater differentiation between populations. Preliminary evidence suggests the rates of sexual reproduction may differ between populations. This study highlights how differences in pathogen populations might be used to identify genes important for survival on crops and how reproduction might impact adaptation. These findings are relevant to all crop-reservoir systems and will remain unnoticed without comparison to wild reservoirs.