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Insight into the composition and function of the tick microbiome has expanded considerably in recent years. Thus far, tick microbiome studies have focused on species and life stages that are responsible for transmitting disease. In this study we conducted extensive field sampling of six tick species in the far-western United States to comparatively examine the microbial composition of sympatric tick species: Ixodes pacificus, Ixodes angustus, Dermacentor variabilis, Dermacentor occidentalis, Dermacentor albipictus, and Haemaphysalis leporispalustris. These species represent both common vectors of disease and species that rarely encounter humans, exhibiting a range of host preferences and natural history. We found significant differences in microbial species diversity and composition by tick species and life stage. The microbiome of most species examined were dominated by a few primary endosymbionts. Across all species, the relative abundance of these endosymbionts increased with life stage while species richness and diversity decreased with development. Only one species, I. angustus, did not show the presence of a single dominant microbial species indicating the unique physiology of this species or its interaction with the surrounding environment. Tick species that specialize in a small number of host species or habitat ranges exhibited lower microbiome diversity, suggesting that exposure to environmental conditions or host blood meal diversity can affect the tick microbiome which in turn may affect pathogen transmission. These findings reveal important associations between ticks and their microbial community and improve our understanding of the function of non-pathogenic microbiomes in tick physiology and pathogen transmission.