HIV‐1‐infected people have an increased risk of developing extrapulmonary tuberculosis (TB), the immunopathogenesis of which is poorly understood. Here, we conducted a detailed immunological analysis of human pericardial TB, to determine the effect of HIV‐1 co‐infection on the phenotype of Mycobacterium tuberculosis (MTB)‐specific memory T cells and the role of polyfunctional T cells at the disease site, using cells from pericardial fluid and blood of 74 patients with (n=50) and without (n=24) HIV‐1 co‐infection. The MTB antigen‐induced IFN‐γ response was elevated at the disease site, irrespective of HIV‐1 status or antigenic stimulant. However, the IFN‐γ ELISpot showed no clear evidence of increased numbers of antigen‐specific cells at the disease site except for ESAT‐6 in HIV‐1 uninfected individuals (p=0.009). Flow cytometric analysis showed that CD4⁺ memory T cells in the pericardial fluid of HIV‐1‐infected patients were of a less differentiated phenotype, with the presence of polyfunctional CD4⁺ T cells expressing TNF, IL‐2 and IFN‐γ. These results indicate that HIV‐1 infection results in altered phenotype and function of MTB‐specific CD4⁺ T cells at the disease site, which may contribute to the increased risk of developing TB at all stages of HIV‐1 infection.