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Many organisms have intimate associations with beneficial microbes acquired from the environment. These host-symbiont associations can be specific and stable, but they are prone to lower partner specificity and more partner-switching than vertically transmitted mutualisms. To investigate partner specificity in an environmentally acquired insect symbiosis, we used 16S rRNA gene and multilocus sequencing to survey the bacterial population in the bacteria-harbouring organ (crypts) of 49 individuals across four sympatric broad-headed bug species (Alydus calcaratus, A. conspersus, A. tomentosus and Megalotomus quinquespinosus). Similar to other insect-bacteria associations, Burkholderia spp. were the most common residents of the crypts in all four insect species (77.2% of recovered sequences). Burkholderia presence was associated with prolonged survival to adulthood in A. tomentosus, suggesting a beneficial role of these specialized associations. Burkholderia were also found in environmental reservoirs in the insects' habitat, which may facilitate acquisition by insects by increasing Burkholderia-insect encounters. Symbiont establishment could also be facilitated by resistance to insect defences; zone of inhibition assays demonstrated that Burkholderia and other bacteria isolated from crypts are resistant to insect defences that limit growth of Escherichia coli. Alternatively, the insects' defences may not efficiently kill a broad range of bacteria. Although the symbiosis is targeted to Burkholderia, the insects' crypts housed other bacteria, including non-Burkholderiaceae species. There is no significant effect of host insect species on Burkholderia distribution, suggesting a lack of strong partner specificity at finer scales. The presence of frequent partner-switching between sympatric insects and their symbionts likely prevents tight co-evolutionary dynamics.