T_H17 cells originating from regulatory T (T_reg) cells upon loss of the T_reg-specific transcription factor Foxp3 accumulate in sites of inflammation and aggravate autoimmune diseases. Whether an active mechanism drives the generation of these pathogenic ‘ex-Foxp3 T_H17’ cells, remains unclear. Here we show that pro-inflammatory cytokines enhance the expression of transcription regulator Id2, which mediates cellular plasticity of T_reg into ex-Foxp3 T_H17 cells. Expression of Id2 in in vitro differentiated iT_reg cells reduces the expression of Foxp3 by sequestration of the transcription activator E2A, leading to the induction of T_H17-related cytokines. T_reg-specific ectopic expression of Id2 in mice significantly reduces the T_reg compartment and causes immune dysregulation. Cellular fate-mapping experiments reveal enhanced T_reg plasticity compared to wild-type, resulting in exacerbated experimental autoimmune encephalomyelitis pathogenesis or enhanced anti-tumor immunity. Our findings suggest that controlling Id2 expression may provide a novel approach for effective T_reg cell immunotherapies for both autoimmunity and cancer.