Many insects acquire beneficial bacterial symbionts from the environment each generation. This may limit co-evolutionary processes that could lead to specialization. Here, leveraging the experimentally tractable symbiosis between squash bugs (Anasa spp.) and their bacterial symbionts, we test for signatures of specialization between bugs and bacteria across populations within a host species and across different host species. We find no evidence for local adaptation between sympatric lineages of Anasa tristis squash bugs and Caballeronia spp. symbionts across their native geographic range; bugs received equal fitness benefits from sympatric symbionts isolated from their location and allopatric symbionts isolated from other regions. We also found no evidence for specialization between three co-localized Anasa host species and their native Caballeronia symbionts. Our results demonstrate generalist dynamics underlie the interaction between Anasa insect hosts and their Caballeronia symbionts, which has implications for the evolution of the symbiosis and for the persistence of beneficial symbioses for these agricultural pests.