Wood-feeding termites harbor specialized wood-feeding protists in their hindguts in a classic nutritional mutualism. The protists are vertically inherited, which has generated a broad-scale pattern of codiversification over ~150 million years, but there are many incongruences due to lineage-specific loss and transfer of symbionts. Despite the economic and evolutionary importance of this symbiosis, the symbiont community compositions most termite species are unknown. We have therefore investigated R. flavipes (Kollar), R. hesperus Banks, and R. tibialis Banks as part of an ongoing effort to understand the diversity and evolutionary history of termite symbionts. We used a single cell PCR approach to link protist morphology to 18S rRNA gene sequences and enable formal classification. The >50 new symbiont species belong to the lineages Trichonympha, Spirotrichonymphida, and Pyrsonymphidae, as expected for Reticulitermes. While Spirotrichonymphida symbionts were fairly well accommodated by existing genera, requiring only 1 new genus, the diversity and phylogeny of Pyrsonymphidae indicated a need for major revision. We have restricted the definitions of Dinenympha and Pyrsonympha to the clades that include their type species, and we propose 6 new genera to accommodate the remaining clades. Community metabarcoding revealed considerable variation in composition across R. tibialis colonies in Arizona, indicative of a symbiont metacommunity. This stands in contrast with the traditional paradigm that each termite species harbors a definitive, limited set of symbiont species. This work was carried out in part as a course-based undergraduate research experience at Arizona State University.