Helminth parasites represent a significant threat to wild, domesticated, and research animal health. Pseudocapillaria tomentosa is a common intestinal nematode parasite and an important source of infection in zebrafish. Symptoms of the infection vary widely from no clinical signs to sever emaciation and mortality, however, the reasons underpinning these disparate outcomes are unclear. Components of the microbiome may interact with parasites to influence their success in the gut while parasite infections are also known to influence the composition of the gut microbiome. In this study we evaluated the longitudinal changes in the gut microbiome structure and gut physiology during experimental P. tomentosa infection in adult 5D line zebrafish. We observed less severe signs of infection and less mortality in these fish than previously described in AB line fish. However, inflammation and epithelial hyperplasia in the intestine was still observed in infected 5D line fish. The composition of the microbiome changed rapidly during the infection and these changes were associated with parasite stage of development and burden. Individual taxa covaried with parasite abundance in the intestine intimating the gut microbiome may influence parasite burden. Associations between taxa and parasite abundance in some cases appeared to be phylogenetically patterned. Strong positive associations were observed between OTUs phylotyped to Proteobacteria and abundance of adult parasites and parasite eggs. Together these experiments demonstrate that P. tomentosa infection results in a rapid and temporally dynamic disruption of the zebrafish gut microbiome and clarify how interactions between the gut microbiome and intestinal parasites may impact fish populations.