Background: Next-generation sequencing has opened new avenues for studying metabolic capabilities of bacteria that cannot be cultured. Here, we provide a metagenomic description of chemoautotrophic gammaproteobacterial symbionts associated with Thyasira cf. gouldi, a sediment-dwelling bivalve from the family Thyasiridae. Thyasirid symbionts differ from those of other bivalves by being extracellular, and recent work suggests that they are capable of living freely in the environment. Results: Thyasira cf. gouldi symbionts appear to form mixed, non-clonal populations in the host, show no signs of genomic reduction and contain many genes that would only be useful outside the host, including flagellar and chemotaxis genes. The thyasirid symbionts may be capable of sulfur oxidation via both the sulfur oxidation and reverse dissimilatory sulfate reduction pathways, as observed in other bivalve symbionts. In addition, genes for hydrogen oxidation and dissimilatory nitrate reduction were found, suggesting varied metabolic capabilities under a range of redox conditions. The genes of the tricarboxylic acid cycle are also present, along with membrane bound sugar importer channels, suggesting that the bacteria may be mixotrophic. Conclusions: In this study, we have generated the first thyasirid symbiont genomic resources. In Thyasira cf. gouldi, symbiont populations appear non-clonal and encode genes for a plethora of metabolic capabilities; future work should examine whether symbiont heterogeneity and metabolic breadth, which have been shown in some intracellular chemosymbionts, are signatures of extracellular chemosymbionts in bivalves.