Oribatid mites are a specious order of microarthropods within the Chelicerata, compromising about 11,000 described species. They are ubiquitously distributed across different microhabitats in all terrestrial ecosystems around the world and were among the first animals colonizing terrestrial habitats as decomposers and scavengers. Despite their species richness and ecological importance genomic resources are lacking for oribatids. Here, we present a 143-Mb chromosome-level genome assembly of the clonal, all-female oribatid mite species Archegozetes longisetosus Aoki, a model species used by numerous laboratories for the past 30 years. Comparative genomic and transcriptional analyses revealed patterns of reduced body segmentation and loss of the segmental identity gene abd-A within Acariformes, and unexpected expression of key eye development genes in these eyeless mites across developmental stages. Consistent with their soil dwelling lifestyle, investigation of sensory genes revealed a species-specific expansion of gustatory receptors, and evidence of horizontally transferred genes related to cell wall degradation of plant and fungal matter, both components of Archegozetes’ diet. Oribatid mites are also noted for their biosynthesis capacities and biochemical diversity. Using biochemical and genomic data, we were able to delineate the backbone biosynthesis of monoterpenes, an important class of compounds found in the major exocrine gland system of Oribatida – the oil glands. Given the mite’s strength as an experimental model, the new high-quality resources provided here will serve as the foundation for molecular research in Oribatida and will enable a broader understanding of chelicerate evolution.