The mucosal barrier of the gastrointestinal tract is essential for maintaining tolerance to the commensal microbiota and protecting the host from pathogenic infections. A vital component of this barrier is secretory IgA (sIgA), which coats up to 70% of the small intestinal microbiota and is the most abundant antibody isotype produced in mammalian gastrointestinal mucosa. sIgA is known to restrict or promote mucosal bacterial colonization, alter bacterial gene expression and metabolism, confer protection against mucosal infections, or neutralize toxins. This suggests that sIgA is crucial in establishing tolerance with the microbiota at the intestinal barrier. Confounding interpretations of IgA function is potential IgM compensation. IgM was reported to coat intestinal microbes in AID deficient mice and IgA deficient humans. These data point to a hypothesis that IgM may compensate for and control the microbiota in conditions of IgA deficiency. Analogous to IgA deficient patients, the original IgA deficient mouse model (Igha-/-) exhibits an increase of serum and mucosal IgM. We developed a novel model of IgA deficiency, IgA secretory deficient mouse (Ighasec-/-), which circumvents increased IgM production. This allowed us to address a long-standing question how IgA maintains immune homeostasis with the microbiota, and whether IgM compensates for IgA deficiency. Using SPF and GF Ighasec-/-, we observed a microbiota dependent expansion of CD8αβ+ intraepithelial lymphocytes (IELs) in the small intestine of IgA deficient mice. These IELs showed features of antigen drive and were licensed by BATF3 dependent dendritic cells. We identified that IgA neutralized murine astrovirus (MuAstV) to limit inflammatory T cell responses in the intestine. In the absence of IgA, MuAstV chronically infected intestinal epithelial cells and drove a CD8αβ+ T cell expansion to limit host interferon responses and viral load. Notably, GC B cells and T cell-dependent IgA were necessary for the host to control MuAstV. In addition, we found that IgA was critical in controlling other enteric viruses, such as murine norovirus strain CR6, and protecting the host from immunopathology. These data identify specific IgA-virome interactions essential for maintaining intestinal immune homeostasis.