Specification of the T helper 17 (Th17) cell lineage requires a well-defined set of transcription factors, but how these integrate with posttranscriptional and epigenetic programs to regulate gene expression is poorly understood. Here we found defective Th17 cell cytokine expression in miR-155-deficient CD4+ T cells in vitro and in vivo. Mir155 was bound by Th17 cell transcription factors and was highly expressed during Th17 cell differentiation. miR-155-deficient Th17 and T regulatory (Treg) cells expressed increased amounts of Jarid2, a DNA-binding protein that recruits the Polycomb Repressive Complex 2 (PRC2) to chromatin. PRC2 binding to chromatin and H3K27 histone methylation was increased in miR-155-deficient cells, coinciding with failure to express Il22, Il10, Il9, and Atf3. Defects in Th17 cell cytokine expression and Treg cell homeostasis in the absence of Mir155 could be partially suppressed by Jarid2 deletion. Thus, miR-155 contributes to Th17 cell function by suppressing the inhibitory effects of Jarid2. Display omitted •miR-155 is highly induced during mouse and human Th17 cell differentiation•Jarid2 and miR-155 are epistatic in Th17 and Treg cells•Jarid2 is required to recruit PRC2 to genomic sites in Th17 cells•Direct targets of PRC2 in Th17 cells include Il22, Il10, Il9, and Atf3 miR-155 is known to promote inflammatory Th17 cell responses, but the mechanism has been unclear. Escobar et al. find that miR-155 promotes cytokine expression in Th17 cells by repressing Jarid2 to relieve Polycomb-mediated gene silencing.