Recent evidence suggests that Helicobacter pylori evades the host immune response by modulating DC activation towards the induction of Tregs, a response that may protect the host from unrelated diseases such as childhood asthma. While immunoregulatory mechanisms are generally accepted as important in determining the outcome of infection, the H. pylori-induced molecular mechanisms triggered in the host and the events that instruct the nature of the ensuing immunopathogenesis remain poorly defined. In this work, we identified a role for IRAK-M in regulating inflammation during Helicobacter infection and hypothesized that IRAK-M expression in dendritic cells limits the host response to H. pylori infection. To evaluate the role of IRAK-M in H. pylori-activation of dendritic cells, we compared the ability of wild type C57BL/6 and IRAK-M-/- BMDCs to express cytokines, costimulation markers, and to influence T cell differentiation in vitro. We found that IRAK-M-/- BMDCs expressed lower levels of IL-10 and PD-L1, and higher levels of MIP-2 and MHC-II, but were comparable to wild type BMDCs in inducing T cell differentiation. To assess the role of IRAK-M in vivo, we infected C57BL/6 and IRAK-M deficient mice with either H. pylori or H. felis and analyzed the host response in both short term and chronic infection settings. Lack of IRAK-M led to increased formation of isolated lymphoid follicles (ILFs) compared to wild type mice chronically infected with H. pylori,or short term H. felis infection. Consistent with increased numbers of ILFs, IRAK-M-/- animals expressed higher levels of CXCL13 and TNFα. Antibody titers in IRAK-M-/- animals chronically infected with H. pylori were also increased compared to wild type infected animals, and the gastric tissue of IRAK-M-/- animals had significantly higher levels of IL-17A and lower levels of IL-10. Finally, we determined that along with previously described CD4+ T cells, ILCs contribute to IL-17A production in the gastric mucosa, and that depletion of ILCs leads to decreased levels of antimicrobial peptide expression. Therefore, in addition to its previously documented role in regulating the host immune response, IRAK-M may play a previously unappreciated role in regulating lymphoid follicle development in the context of Helicobacter infection.