CD4⁺ T cell expression of IL‐10 is an important mechanism controlling immunity to tuberculosis (TB). To identify the CD4⁺ T cell subsets producing IL‐10 in human TB, we enumerated the frequencies of IL‐10 expressing CD4⁺ T cell subsets following TB—antigen stimulation of cells from individuals with pulmonary (PTB) and latent TB (LTB). We first demonstrate that TB antigens induce an expansion of IL‐10 expressing Th1 (IL‐10⁺, IFNγ⁺, T‐bet⁺), Th2 (IL‐10⁺, IL‐4⁺, GATA‐3⁺), Th9 (IL‐10⁺, IL‐9⁺, IL‐4⁻), Th17 (IL‐10⁺, IL‐17⁺, IFNγ⁻), and natural and adaptive regulatory T cells [nTregs; IL‐10⁺, CD4⁺, CD25⁺, Foxp3⁺ and aTregs; IL‐10 single⁺, CD4⁺, CD25⁻, Foxp3⁻] in PTB and LTB individuals, with frequencies being significantly higher in the former. However, only Th1 cells and adaptive Tregs expressing IL‐10 exhibit a positive relationship with bacterial burdens and extent of disease in PTB. Finally, we show that IL‐27 and TGFβ play an important role in the regulation of IL‐10⁺ Th cell subsets. Thus, active PTB is characterized by an IL‐27 and TGFβ mediated expansion of IL‐10 expressing CD4⁺ T cell subsets, with IL‐10⁺ Th1 and IL‐10⁺ aTreg cells playing a potentially pivotal role in the pathogenesis of active disease.