Bacteria in the honeybee gut have garnered much attention as a factor affecting bee health. However, unlike the hindgut, which has been the primary focus of this research, the crop, or the honey stomach, is often assumed to be dominated by environmentally acquired transient taxa that matter little to the bees. To evaluate this assumption, we examined bacterial taxa in the crop and the mouth of foraging adults of Apis mellifera and A. cerana japonica and the floral nectar of the Japanese apricot, Prunus mume, visited by the bees in the Minabe-Tanabe region of Japan. We found that the crop was distinct from both the mouth and the nectar in bacterial composition even though all samples were collected simultaneously at the same locations, whereas mouth and nectar samples were indistinguishable from each other. Furthermore, the crop remained similar in bacterial composition and alpha and beta diversity from summer to winter, whereas the mouth showed a sharp drop in alpha diversity and a large increase in beta diversity from summer to winter. These results refute the conventional assumption, suggesting instead that the crop contains a conserved bacterial community that is largely distinct from the environmental taxa that the bees encounter as they forage in the environment. We also found, however, that strains of a representative crop-associated species, Apilactobacillus kunkeei, could be season- and host species-specific. Together, these findings suggest that further studies of crop-associated bacterial communities are needed to better understand the relationship between honeybees and their gut bacteria.