Allergens are typically studied from the perspective of the human immune system, with research focusing on the molecular and genetic mechanisms underlying hypersensitivity to otherwise benign environmental proteins. Yet allergenicity is unlikely to be an evolved trait in the source organisms themselves. Rather, it may be a byproduct of proteins shaped by ecological adaptations. Despite this possibility, the role of ecological transitions in shaping allergenic potential remains poorly understood. Pyroglyphid house dust mites (HDM) offer a unique opportunity to explore this question. These mites evolved from parasitic skin mites and transitioned to a free-living lifestyle in bird and mammal nests millions of years ago. A subset of species later colonized human dwellings, becoming the predominant source of indoor allergens. This reversal from parasitism to free-living is rare among animals and may have imposed novel selective pressures on HDM physiology, including proteins now known to act as allergens. We analyzed the genomic signatures associated with this transition using a phylogenomic dataset of 54 pyroglyphid HDM species and relatives. Our time-calibrated phylogeny suggests HDM diverged from parasitic ancestors 47 million years ago, with two independent reversals to parasitism within the lineage. We curated orthologs for 38 known HDM allergen groups and assessed gene copy number variation, sequence evolution, selection pressures, domain structure, and synteny. Preliminary results reveal positive selection on genes related to proteolysis and housekeeping in parasitic ancestors, consistent with Red Queen dynamics. In contrast, free-living HDM show enrichment in lipid-binding protein families likely involved in immune defense and microbial resistance. This aligns with observations that some lineages, including Dermatophagoides farinae, are heavily infected with the endosymbiotic bacterium Cardinium. Together, our findings suggest that HDM allergenicity has been shaped by both parasitic and free-living states, with inadvertent consequences for human allergic responses.