Changes to the symbiotic microbiota early in life, or the absence of it, can lead to exacerbated type 2 immunity and allergic inflammations. While it is unclear how the microbiota regulates type 2 immunity, it is a strong inducer of pro-inflammatory T helper (Th) 17 cells and regulatory T cells (Tregs) in the intestine. Here, we report that microbiota-induced Tregs express the nuclear hormone receptor RORγt and differentiate along a pathway that also leads to Th17 cells. In the absence of RORγt(+) Tregs, Th2-driven defense against helminths is more efficient while Th2-associated pathology is exacerbated. Thus, the microbiota regulates type 2 responses through the induction of "type 3" RORγt(+) Tregs and Th17 cells and acts as a key factor in balancing immune responses at mucosal surfaces.