The wheat curl mite (WCM), Aceria tosichella Keifer, is a major pest of cereals worldwide that also comprises a complex of at least 16 genetic lineages with divergent physiological traits, including host associations and specificity. The goal of this study was to test the extent to which host-plant species and landscape spatial variation influence WCM presence and population density across the entire area of Poland (>311,000 km2). Three important findings arose from the results of the study. (1) The majority of WCM lineages analyzed exhibited variation in patterns of prevalence and/or population density on both spatial and host-associated scales. (2) Areas of occurrence and local abundance were delineated for specific WCM lineages and it was determined that the most pestiferous lineages are much less widespread than was expected, suggesting relatively recent introductions into Poland and the potential for further spread. (3) The 16 WCM lineages under study assorted within four discrete host assemblages, within which similar host preferences and host infestation patterns were detected. Of these four groups, one consists of lineages associated with cereals. In addition to improving basic ecological knowledge of a widespread arthropod herbivore, the results of this research identify high-risk areas for the presence of the most pestiferous WCM lineages in the study area (viz. the entirety of Poland). They also provide insight into the evolution of pest species of domesticated crops and facilitate testing of fundamental hypotheses about the ecological factors that shape this pest community.