How parasites alter host feeding ecology remains elusive in natural populations. A powerful approach to investigate the link between infection and feeding ecology is quantifying unique and shared responses to parasite infection in related host species within a common environment. Here, 9 pairs of sympatric populations of the three-spined and nine-spined stickleback fishes were sampled across a range of freshwater and brackish habitats to investigate how parasites alter host feeding ecology: (i) biotic and abiotic determinants of parasite community composition, and (ii) to what extent parasite infection correlates with trophic niche specialization of the 2 species, using stable isotope analyses (δ15N and δ13C). It was determined that parasite community composition and host parasite load varied among sites and species and were correlated with dissolved oxygen. It was also observed that the digenean Cyathocotyle sp.'s abundance, a common directly infecting parasite with a complex life cycle, correlated with host δ13C in a fish species-specific manner. In 6 sites, correlations were found between parasite abundance and their hosts' feeding ecology. These effects were location-specific and occasionally host species or host size-specific. Overall, the results suggest a relationship between parasite infection and host trophic niche which may be an important and largely overlooked ecological factor. The population specificity and variation in parasite communities also suggest this effect is multifarious and context-dependent.