Production of autoantibodies and Immunoglobulin E (IgE) by B lymphocytes triggers autoimmune and allergic diseases, and consequently is actively suppressed. Patients with Autoimmune Lymphoproliferative Syndrome (ALPS) due to mutation of the death receptor Fas develop autoantibodies, which has been presumed to result from the failure of Fas-mediated deletion of self-reactive germinal center (GC) B cells. Here we show that Fas is in fact not required for the purging of self-reactive GC B cells. Instead, Fas-deficiency leads to the emergence of "rogue" GC B cells that escape negative selection and differentiate into clonally restricted pools of antibody-secreting plasma cells that include 100-fold increased numbers of IgE+ plasma cells. Significantly, a major cohort of ALPS patients was also found to have high levels of serum IgE. These results redefine the role of Fas in counteracting autoimmunity and reveal Fas to have a B cell intrinsic function in suppressing IgE antibody responses in both humans and mice.