T follicular helper cells (T FH) are critical for the development and maintenance of germinal center (GC) and humoral immune responses. During chronic HIV/SIV infection, T FH accumulate, possibly as a result of Ag persistence. The HIV/SIV-associated T FH expansion may also reflect lack of regulation by suppressive follicular regulatory CD4+ T cells (T FR). T FR are natural regulatory T cells (T REG) that migrate into the follicle and, similar to T FH, upregulate CXCR5, Bcl-6, and PD1. In this study, we identified T FR as CD4+ CD25+ FOXP3+ CXCR5+ PD1 hi Bcl-6+ within lymph nodes of rhesus macaques (RM) and confirmed their localization within the GC by immunohistochemistry. RNA sequencing showed that T FR exhibit a distinct transcriptional profile with shared features of both T FH and T REG, including intermediate expression of FOXP3, Bcl-6, PRDM1, IL-10, and IL-21. In healthy, SIV-uninfected RM, we observed a negative correlation between frequencies of T FR and both T FH and GC B cells, as well as levels of CD4+ T cell proliferation. Post SIV infection, the T FR/T FH ratio was reduced with no change in the frequency of T REG or T FR within the total CD4+ T cell pool. Finally, we examined whether higher levels of direct virus infection of T FR were responsible for their relative depletion post SIV infection. We found that T FH, T FR, and T REG sorted from SIV-infected RM harbor comparable levels of cell-associated viral DNA. Our data suggest that T FR may contribute to the regulation and proliferation of T FH and GC B cells in vivo and that a decreased T FR/T FH ratio in chronic SIV infection may lead to unchecked expansion of both T FH and GC B cells.