Wood-feeding termites harbor specialized 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 evolutionary and economic importance of this symbiosis, the symbiont communities of most termite species are incompletely characterized or entirely unstudied. Here, we have investigated the protist symbiont community of Reticulitermes tibialis, using single-cell PCR to link morphology to 18S rRNA gene sequences. The protists belong to at least 41 species in 3 major lineages within Metamonada: Spirotrichonymphida, Pyrsonymphidae, and Trichonympha. The Spirotrichonymphida symbionts belong to 6 genera, including Pseudospironympha, which has not been found in Reticulitermes until now, and Dexiohelix, a new genus. Pyrsonymphidae traditionally include just Pyrsonympha and Dinenympha, but our morphology-linked 18S phylogeny indicates that both genera are polyphyletic. We accordingly restrict the definitions of Pyrsonympha and Dinenympha to the clades that include their type species, and we propose 5 new genera to accommodate the remaining clades. Short-read 18S amplicon sequencing revealed considerable variation in community composition across R. tibialis colonies in Arizona, suggestive of a symbiont metacommunity. Symbiont species varied in their prevalence across colonies, with a core set of about 12 highly prevalent symbiont species, 11 species with intermediate prevalence, and 18 rare species. This pattern contrasts with the traditional paradigm of consistent symbiont community composition across colonies of a termite species.