HIV-infected individuals are significantly more susceptible to tuberculosis (TB) than HIV-uninfected individuals. Although it is established that HIV reduces M. tuberculosis-specific T cell responses, the causes of this dysfunction are not known. We used the cynomolgus macaque model of TB to demonstrate that ex vivo SIV reduces the frequency of M. tuberculosis-specific TNF and IFN-γ producing T cells within 24hrs post-infection. In vivo, T cell IFN-γ responses in granulomas from animals with SIV/M. tuberculosis co-infection were lower than SIV-negative animals with active TB. The SIV effects on inhibition of T cell responses were primarily on antigen presenting cells and not the T cells directly. Specifically, reductions in the frequency of TNF-producing M. tuberculosis-specific CD4 T cells were caused, at least in part, by SIV-induced production of monocyte derived IL-5.