Bathymodiolin mussels dominate hydrothermal vent and cold seep communities worldwide. Symbiotic associations with chemosynthetic sulfur- and methane-oxidizing bacteria that provide for their nutrition are the key to their ecological and evolutionary success. The current paradigm is that these symbioses evolved from two free-living ancestors, one methane-oxidizing and one sulfur-oxidizing bacterium. In contrast to previous studies, our phylogenetic analyses of the bathymodiolin symbionts show that both the sulfur and the methane oxidizers fall into multiple clades interspersed with free-living bacteria, many of which were discovered recently in metagenomes from marine oxygen minimum zones. We therefore hypothesize that symbioses between bathymodiolin mussels and free-living sulfur- and methane-oxidizing bacteria evolved multiple times in convergent evolution. Furthermore, by 16S rRNA sequencing and fluorescence in situ hybridization, we show that close relatives of the bathymodiolin symbionts occur on hosts belonging to different animal phyla: Raricirrus beryli, a terebellid polychaete from a whale-fall, and a poecilosclerid sponge from a cold seep. The host range within the bathymodiolin symbionts is therefore greater than previously recognized, confirming the remarkable flexibility of these symbiotic associations.