Changes to the symbiotic microbiota early in life, or the absence of it, can lead to exacerbated type 2 immunity and allergic inflammations. Although it is unclear how the microbiota regulates type 2 immunity, it is a strong inducer of proinflammatory T helper 17 (T_H17) cells and regulatory T cells (T_regs) in the intestine. Here, we report that microbiota-induced T_regs express the nuclear hormone receptor RORγt and differentiate along a pathway that also leads to T_H17 cells. In the absence of RORγt⁺ T_regs, T_H2-driven defense against helminths is more efficient, whereas T_H2-associated pathology is exacerbated. Thus, the microbiota regulates type 2 responses through the induction of type 3 RORγt⁺ T_regs and T_H17 cells and acts as a key factor in balancing immune responses at mucosal surfaces.