Fas‐associated protein with death domain/mediator of receptor induced toxicity (FADD/MORT1) was first described as a transducer of death receptor signalling but was later recognized also to be important for proliferation of T cells. B‐cell lymphoma 3 (Bcl‐3) is a relatively little understood member of the nuclear factor (NF)‐κB family of transcription factors. We recently found that Bcl‐3 is up‐regulated in T cells from mice where FADD function is blocked by a dominant negative transgene (FADD‐DN). To understand the importance of this, we generated FADD‐DN/bcl‐3^−/− mice. Here, we report that T cells from these mice show massive cell death and severely reduced proliferation in response to T‐cell receptor (TCR) stimulation in vitro. Transgenic co‐expression of Bcl‐2 (FADD‐DN/bcl‐3^−/−/vav‐bcl‐2 mice) rescued the survival but not the proliferation of T cells. FADD‐DN/bcl‐3^−/− mice had normal thymocyte numbers but reduced numbers of peripheral T cells despite an increase in cycling T cells in vivo. However, activation of the classical NF‐κB and extracellular regulated kinase (ERK) pathways and expression of interleukin (IL)‐2 mRNA upon stimulation were normal in T cells from FADD‐DN/bcl‐3^−/− mice. These data suggest that FADD and Bcl‐3 regulate separate pathways that both contribute to survival and proliferation in mouse T cells.