High densities of the wood-boring bivalve Xylophaga atlantica colonized pine wood cubes in colonization devices deployed at 2279 m depth for 414 days (14 July 2007–31 August 2008) near hydrothermal vents at the Rainbow site on the Mid-Atlantic Ridge (36°13.7454′N/33°54.0513′W). Histological and biometric observations on specimens with shell lengths (SLs) of 0.5–4.2 mm revealed three cohorts in this dioecious population. The first cohort was dominated by mature females, each with an estimated fecundity of ~450 oocytes with a mean diameter of 28.0 ± 3.9 µm (maximum diameter 40.0 µm); an intermediate cohort was a mix of males and females with SL at first maturity of ≤1.7 mm; the third cohort was exclusively morphologically distinct, mature, dwarf males, SL ~500 µm. These dwarf males were attached to the dorsal shell surfaces of females in the first cohort. The difference in the SL of Prodissoconch I (~60 µm) and Prodissoconch II (500–530 µm) confirmed planktotrophy. Based on their carbon and nitrogen stable isotope ratios, and a paedomorphic morphology suggesting they are ill-equipped to bore wood, it seems likely that the dwarf males are heterotrophic filter-feeders. Fluorescence in situ hybridization showed, however, that dwarf males hosted a few Gammaproteobacteria in their gills. The absence of a bacterial signal in the germ cells and developing oocytes of females implies that direct trans-ovarial inheritance of symbiotic bacteria does not occur in X. atlantica.