The gut microbiome of bees is vital for the health of their hosts. Given the ecosystem functions performed by bees, and the declines faced by many species, it is important to improve our understanding of the amount of natural variation in the gut microbiome, the level of sharing of bacteria among co-occurring species (including between native and non-native species), and how gut communities respond to infections. We conducted 16S rRNA metabarcoding to discern the level of microbiome similarity between honey bees (Apis mellifera,N= 49) and bumble bees (Bombusspp.,N= 66) in a suburban-rural landscape. We identified a total of 233 amplicon sequence variants (ASVs) and found simple gut microbiomes dominated by bacterial taxa belonging toGilliamella,Snodgrassella, andLactobacillus. The average number of ASVs per species ranged from 4.00–15.00 (8.79 ± 3.84, mean ± SD). Amplicon sequence variant of one bacterial species,G. apicola(ASV 1), was widely shared across honey bees and bumble bees. However, we detected another ASV ofG. apicolathat was either exclusive to honey bees, or represented an intra-genomic 16S rRNA haplotype variant in honey bees. Other than ASV 1, honey bees and bumble bees rarely share gut bacteria, even ones likely derived from outside environments (e.g.,Rhizobiumspp.,Fructobacillusspp.). Honey bee bacterial microbiomes exhibited higher alpha diversity but lower beta and gamma diversities than those of bumble bees, likely a result of the former possessing larger, perennial hives. Finally, we identified pathogenic or symbiotic bacteria (G. apicola,Acinetobactersp. andPluralibactersp.) that associate with Trypanosome and/orVairimorphainfections in bees. Such insights help to determine bees’ susceptibility to infections should gut microbiomes become disrupted by chemical pollutants and contribute to our understanding of what constitutes a state of dysbiosis.