The gut microbiome regulates multiple aspects of host health, including metabolism and the development of the immune system. Despite this, we still know relatively little about how the gut microbiome influences host responses to parasitism in wild organisms, particularly whether interactions between gut microbiota and host physiology contribute to variation in parasitism across host species. The goal of this study was to determine the role of gut microbiota in shaping how birds respond to nest parasites and investigate whether this relationship varies between host species. Both eastern bluebirds (Sialia sialis) and tree swallows (Tachycineta bicolor) are parasitized by blow flies (Protocalliphora sialia) which produce larvae that feed on nestlings’ blood. We experimentally manipulated the gut microbiota of nestling bluebirds and tree swallows by dosing nestlings with an oral antibiotic or sterile water as a control. We then quantified nestling physiology (hemoglobin, glucose, parasite specific IgY antibodies), body morphometrics, and survival until fledging, as well as nest parasite abundance and size. We found that an experimental disruption of nestling gut microbiota increased parasite abundance in tree swallows, but decreased parasite abundance in bluebirds. Treatment with antibiotics was associated with delayed parasite development, including reduced pupation volume of parasites found as larvae in bluebird nests. Similarly, antibiotic treatment was associated with larger size differences in pupal volume between parasites found as larvae and pupae in swallow nests. Both antibiotic treatment and parasite abundance had variable effects on nestling body morphometrics and physiology across the two host species. Together, these results suggest that gut microbiota contribute to host differences in resistance to P. sialia and can influence host-parasite interactions.