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Abstract Virus symbionts are important mediators of ecosystem function, yet we know little of their diversity and ecology in natural populations. The alarming decline of pollinating insects in many regions of the globe, especially the European honey bee, Apis mellifera, has been driven in part by worldwide transmission of virus pathogens. Previous work has examined the transmission of known honey bee virus pathogens to wild bee populations, but only a handful of studies have investigated the native viromes associated with wild bees, limiting epidemiological predictors associated with viral pathogenesis. Further, variation among different bee species might have important consequences in the acquisition and maintenance of bee-associated virome diversity. We utilized comparative metatranscriptomics to develop a baseline description of the RNA viromes associated with wild bee pollinators and to document viral diversity, community composition, and structure. Our sampling includes five wild-caught, native bee species that vary in social behavior as well as managed honey bees. We describe 26 putatively new RNA virus species based on RNA-dependent RNA polymerase phylogeny and show that each sampled bee species was associated with a specific virus community composition, even among sympatric populations of distinct host species. From 17 samples of a single host species, we recovered a single virus species despite over 600 km of distance between host populations and found strong evidence for isolation by distance in associated viral populations. Our work adds to the small number of studies examining viral prevalence and community composition in wild bees.