The tumor microenvironment counters antitumor T cell responses in part by blunting their activation and infiltration. Ligands that engage Toll-like receptors (TLR) on T cells and antigen-presenting cells can act as potent immune adjuvants. In this study, we show how tumor-reactive T cells engineered to secrete bacterial flagellin, a TLR5 ligand (TLR5L), can engender a co-stimulatory signal that augments antitumor activity. Human T cells engineered to express TLR5L along with DMF5, a T cell receptor that recognizes the melanoma antigen MART-127-35 (DMF5TLR5L T cells), displayed increased proliferation, cytokine production and cytolytic activity against melanoma cells. In a xenogenetic model, adoptive transfer of DMF5TLR5L T cells reduced tumor growth kinetics and prolonged mouse survival. In a syngeneic model, similarly engineered melanoma-reactive T cells (pmelTLR5L) displayed a relative increase in antitumor activity against established tumors, compared to unmodified T cells. In this model, we documented increased T cell infiltration associated with increased levels of CCR1 and CXCR3 levels on T cells, a reduction in PD1+Lag3+ T cells and CD11+Gr1+ myeloid-derived suppressor cells, and changes in the chemokine/cytokine profile of tumors. Our findings show how T cell-mediated delivery of a TLR agonist to the tumor site can contribute to antitumor efficacy, in the context of adoptive T cell immunotherapy.