FOXP3+ regulatory T (Treg) cells suppress responses to maintain immunological tolerance, but can also impair immunity to infections and cancer. Despite their importance, mechanisms that control Treg cell survival during critical stages of inflammation remain unclear. We found that Treg cell-specific deletion of caspase 8 increased Treg cell number in steady-state, revealing a requirement for death receptor mediated apoptosis for their homeostasis. However, inflammation caused a precipitous drop in caspase-8-deficient Treg cell number, via the induction of the pseudokinase MLKL and subsequent necroptosis. This loss of Treg cells enhanced clearance of herpes virus infection and improved virological control in mice with overwhelming LCMV docile infection, at the expense of lethal autoimmunity in some animals. Furthermore, Treg cells from humans were more sensitive to pharmacological induction of necroptosis than other lymphocyte populations. Therefore, this dual role for caspase 8 in Treg cell apoptosis at steady-state versus protection from necroptosis during inflammation may represent a targetable switch to manipulate Treg cell numbers for therapeutic benefit.