Microsporidia are ubiquitous obligate intracellular pathogens of animals. These parasites often infect hosts through an oral route, but little is known about the function of host intestinal proteins that facilitate microsporidia invasion. To identify such factors necessary for infection by <i>Nematocida parisii</i>, a natural microsporidian pathogen of <i>Caenorhabditis</i> <i>elegans</i>, we performed a forward genetic screen to identify mutant animals that have a Fitness Advantage with <i>Nematocida</i> (Fawn). We isolated four <i>fawn</i> mutants that are resistant to <i>Nematocida</i> infection and contain mutations in <i>T14E8.4</i>, which we renamed <i>
aaim-1</i> (Antibacterial and Aids invasion by Microsporidia). Expression of AAIM-1 in the intestine of <i>
aaim-1</i> animals restores <i>N. parisii</i> infectivity and this rescue of infectivity is dependent upon AAIM-1 secretion. <i>N. parisii</i> spores in <i>
aaim-1</i> animals are improperly oriented in the intestinal lumen, leading to reduced levels of parasite invasion. Conversely, <i>
aaim-1</i> mutants display both increased colonization and susceptibility to the bacterial pathogen <i>Pseudomonas aeruginosa</i> and overexpression of <i>AAIM-1</i> reduces <i>P. aeruginosa</i> colonization. Competitive fitness assays show that <i>
aaim-1</i> mutants are favoured in the presence of <i>N. parisii</i> but disadvantaged on <i>P. aeruginosa</i> compared to wild type animals<i>.</i> Together, this work demonstrates how microsporidia exploits a secreted protein to promote host invasion. Our results also suggest evolutionary trade-offs may exist to optimizing host defense against multiple classes of pathogens.