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ABSTRACT Organisms inhabiting extreme environments must tolerate a variety of physiochemical stressors. In some cases, host‐associated microbial communities facilitate the survival of their hosts in extreme environments, but extremophile symbioses have not been identified in vertebrates. We used 16S rRNA amplicon sequencing to investigate commonalities and differences in the gut bacterial communities of livebearing fishes (Poecilia mexicanaspecies complex, Poeciliidae) that have repeatedly colonised toxic sulfide streams in southern Mexico. We found shared gut microbial taxa across habitat types and drainages but also differences in the microbiomes between sulfidic and nonsulfidic populations, both in terms of patterns of diversity and community composition. Most importantly, we documented convergent changes in microbiome composition across evolutionarily independent sulfide spring lineages. These patterns were consistent when we analysed the gut microbiomes as well as primarily host‐associated microbiomes that excluded taxa that are commonly found in the environment. Our analyses also revealed several microbial taxa associated with sulfide spring coloniation that have previously been implicated in symbioses and may influence the host's tolerance to the extreme environmental conditions. Our study sheds light on how shared environmental pressures can give rise to convergent host‐microbiome associations in fishes, and it provides a foundation for investigating the role of host‐microbiome interactions in vertebrate adaptation to extreme environments.