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Many invertebrates at deep-sea hydrothermal vents depend upon bacterial symbionts for nutrition, and thus the mechanism of symbiont transmission, vertical (via the egg or sperm) or horizontal (from environment or contemporary hosts) is critically important. Under a strict maternal transmission model, symbiont and host mitochondrial genomes pass through the same individuals leading to congruent host–symbiont phylogenies. In contrast, horizontally transmitted symbionts are environmentally acquired, leading to incongruent host–symbiont phylogenies. Each of these transmission strategies is predicted to have different consequences for symbiont ecology and genome evolution. Deep-sea mussels (Bathymodiolinae) are globally distributed at deep-sea hydrothermal vents, depend upon chemoautotrophic symbionts for their survival, and are hypothesized to transmit their symbionts horizontally. This study explored bathymodioline symbiont ecology through quantification of symbionts at two hydrothermal vent sites and symbiont evolution using functional gene phylogenies. These phylogenies revealed a dramatically more complex evolutionary history than 16S ribosomal RNA phylogenies, suggesting that horizontal gene transfer may have played an important role in symbiont gene evolution. Tests of the strict maternal transmission hypothesis found that host–symbiont lineages were significantly decoupled across multiple genes. These findings expand our understanding of symbiont ecology and evolution, and provide the strongest evidence yet for horizontal transmission of bathymodioline symbionts.