Specific gut commensal bacteria improve host health by eliciting mutualistic regulatory T (T) cell responses. However, the bacteria that induce effector T (T) cells during inflammation are unclear. We addressed this by analyzing bacterial-reactive T cell receptor (TCR) transgenic cells and TCR repertoires in a murine colitis model. Unexpectedly, we found that mucosal-associated species triggered both T cell responses during homeostasis and T cell responses during colitis, as suggested by an increased overlap between the T/T TCR repertoires with colitis. Four of six T TCRs tested recognized mucosal-associated species in vitro and in vivo. By contrast, the marked expansion of luminal species seen during colitis did not trigger a commensurate T cell response. Unlike other T cell-inducing bacteria, species are known pathobionts and cause disease in immunodeficient mice. Thus, our study suggests a model in which mucosal bacteria elicit context-dependent T or T cell responses to facilitate intestinal tolerance or inflammation.