Although enriched in normal intestines, the role of CD4+ Th17 cells in regulation of the host response to microbiota, and whether and how they contribute to intestinal homeostasis is still largely unknown. It is also unclear whether Th17 cells regulate intestinal IgA production, which is also abundant in the intestinal lumen and plays a crucial role as the first defense line in host response to microbiota. In this study, we found that intestinal polymeric Ig receptor (pIgR) and IgA production was impaired in T cell-deficient TCRβxδ−/− mice. Repletion of TCRβxδ−/− mice with Th17 cells from CBir1 flagellin TCR transgenic mice, which are specific for a commensal antigen, increased intestinal pIgR and IgA. The levels of intestinal pIgR and IgA in B6.IL-17 receptor (IL-17R−/−) mice were lower than wild-type mice. Treatment of colonic epithelial HT-29 cells with IL-17 increased pIgR expression. IL-17R−/− mice demonstrated systemic anti-microflora antibody response. Consistently, administering dextran sulfate sodium (DSS) to C57BL/6 mice after treatment with IL-17-neutralizing antibody resulted in more severe intestinal inflammation as compared to control antibody. Administering DSS to IL-17R−/− mice resulted in increased weight loss and more severe intestinal inflammation compared to wild-type mice, indicating a protective role of Th17 cells in intestinal inflammation. Individual mice with lower levels of pIgR and intestinal secreted IgA correlated with increased weight loss at the end of DSS administration. Collectively, our data reveal that microbiota-specific Th17 cells contribute to intestinal homeostasis by regulating intestinal pIgR expression and IgA secretion.