Human and simian immunodeficiency viruses (HIV and SIV) exploit follicular lymphoid regions by establishing high levels of viral replication and dysregulating humoral immunity. Follicular regulatory T cells (T_FR) are a recently characterized subset of lymphocytes that influence the germinal centre response through interactions with follicular helper T cells (T_FH). Here, utilizing both human and rhesus macaque models, we show the impact of HIV and SIV infection on T_FR number and function. We find that T_FR proportionately and numerically expand during infection through mechanisms involving viral entry and replication, TGF-β signalling, low apoptosis rates and the presence of regulatory dendritic cells. Further, T_FR exhibit elevated regulatory phenotypes and impair T_FH functions during HIV infection. Thus, T_FR contribute to inefficient germinal centre responses and inhibit HIV and SIV clearance.