The wheat curl mite (WCM) is a major pest in cereal crops around the world and the vector of at least four known pathogens capable of reducing yields in crops such as wheat, corn, barley, oats, millet and rye. Current taxonomy recognizes WCM as a single species, Aceria tosichella; however, recent genetic, physiological and ecological studies have shown that WCM is likely to be a species complex. In this study we assessed genetic variation and phylogenetic relationships among WCM from four continents and a wide range of host plants using DNA sequence data from one mitochondrial gene, one nuclear gene and a single nuclear intergenic spacer region. Phylogenetic analyses revealed 11 unique mite lineages associated with specific plant hosts including wheat and barley. Host associations were consistent across continents, often with a single haplotype dominating a host plant regardless of geographic origin. The genetic and ecological differences identified in this study support the notion that WCM is a species complex in need of major taxonomic revision. These findings have implications for control of WCM globally, particularly within the context of identifying plants that form 'green bridge' refuges, assessing disease transmission risk, and identifying resistance in cereal genotypes to WCM and associated pathogens.