Organisms inhabiting methane seep sediments are exposed to stress in the form of high levels of hydrogen sulfide, which result mainly from sulfate reduction coupled to anaerobic methane oxidation. Dorvilleidae (Polychaeta) have successfully invaded this ecosystem, and multiple species in divergent genetic clades co-occur at high densities. At methane seeps in the NE Pacific off California and Oregon, the genera Ophryotrocha, Parougia and Exallopus are especially well represented. To test the hypothesis that dorvilleid coexistence is facilitated by niche partitioning through sulfide tolerance and trophic patterns, we examined dorvilleid species-specific patterns of occurrence and nutrition at methane seeps off Eel R. [ER] on the Californian continental slope and at Hydrate Ridge [HR] on the Oregon continental slope, and in two habitats (clam bed and microbial mat) characterized by lower and higher hydrogen sulfide levels, respectively. Microelectrode measurements of hydrogen sulfide enabled characterization of environmental sulfide levels for species sampled in background sediment cores and in colonization trays. Dorvilleids tolerated H2S levels from 10μM to over 2.6mM, with the majority of species inhabiting sediments with similar environmental H2S concentrations (median 85–100μM). Dorvilleid species richness was greater at HR than ER, but did not differ between clam bed and microbial mat habitats. Species distribution patterns reflected preferences for ER clam bed (lower sulfide levels), ER mat and HR clam bed (moderate sulfide levels), or HR mat (very high sulfide levels). Nutritional patterns, including trophic diversity and functional similarity, were examined using community stable isotope metrics based on δ15N and δ13C. Within each region, dorvilleid species exhibited multiple trophic strategies. Co-existing congeners typically exhibited distinct isotope signatures, suggesting trophic partitioning. Trophic diversity and δ15N range for whole assemblages (measured by Total Hull Area and Standard Elliptical Area using species averages) and functional redundancy or species packing (measured as distance to nearest neighbor) among species and individuals were generally higher at ER, where sulfide levels were lower than at HR. In contrast, average trophic diversity among individuals within a species was greater at HR than ER. In colonization experiments involving agar-based manipulations of sulfide in tray sediments that mimicked clam bed and mat conditions, dorvilleids comprised 68% and 48% of colonists at ER and HR, respectively. Dorvilleid species richness was higher in trays that were initially more sulfidic. However, habitat exerted stronger influence on the composition of colonizing dorvilleids than did sulfide additions. In the NE Pacific, regional, habitat and vertical (down-core) variation in hydrogen sulfide creates complex environmental heterogeneity at methane seeps, promoting high diversity of stress-tolerant taxa such as dorvilleid polychaetes.