The life cycle of effector T cells is determined by signals downstream of the T cell receptor (TCR) that induce activation and proinflammatory activity, or death as part of the process to resolve inflammation. We recently reported that T cell myeloid differentiation primary response 88 (MyD88) tunes down TCR activation and limits T cell survival in the cardiac and tumor inflammatory environments, in contrast to its proinflammatory role in myeloid cells upon toll-like receptor (TLR) recognition of pathogen- and damage-associated molecular patterns. However, the molecular mechanism remains unknown. Here, we report a central regulatory role for MyD88 in T cell apoptosis after TCR activation and Fas ligation through an association with the B cell adaptor for phosphoinositide 3-kinase (B cell activating protein [BCAP]). We show that TCR engagement upregulates MyD88 and BCAP and promotes their interaction, thereby limiting availability of BCAP for downstream TCR-BCAP-PI3K-AKT signaling required for T cell activation and survival, which are enhanced in MyD88-/- activated T cells. Further, MyD88 and BCAP association and localization to the TCR was prevented by lipopolysaccharide (LPS) activation of TLR4 and restored T cell survival in wild-type cells. The enhanced T cell activation markers, proinflammatory signals, and survival advantage observed in MyD88-/- T cells was fully eliminatedef upon BCAP knockdown in T cells. Our data demonstrate that MyD88 acts downstream of the TCR to regulate T cell fate through its association with BCAP and elucidate a novel molecular mechanism for MyD88 in T cell biology that could be targeted to fine-tune T cell effector function and survival therapeutically.