The gut microbiota of bees affect nutrition, immunity, and host fitness, yet the role of diet, sociality, and geographic variation in determining microbiome structure, including strain-level diversity and relatedness, remain poorly understood. Here, we use full-length 16S amplicon sequencing to compare the crop and gut microbiomes of two incipiently social carpenter bee species, Xylocopa sonorina and Xylocopa tabaniformis, from multiple geographic sites within each species’ range. We found that Xylocopa species share a set of core taxa consisting of Bombilactobacillus, Bombiscardovia, and Lactobacillus apis, found in >95% of all individual bees sampled, and Gilliamella and Apibacter were also detected in the gut of both species with high frequency. The crop bacterial community of both species was comprised nearly entirely of Apilactobacillus with occasionally abundant nectar bacteria. Despite sharing core taxa, Xylocopa species’ microbiomes were distinguished by multiple bacterial lineages, including species-specific strains of core taxa. In both bee species, bacterial species exhibited geographic patterns in the presence of specific sequence variants. The use of long-read amplicons revealed otherwise cryptic species and population-level differentiation in core microbiome members which was masked when a shorter fragment of the 16S (V4) was considered. We conclude that these Xylocopa species host a distinctive microbiome, similar to that of previously characterized social apids, which suggests that further investigation to understand the evolution of bee microbiome and its drivers is warranted.