Abstract Intratumoral lymph node (LN)-like vasculature, characterized by the expression of peripheral node addressin (PNAd) and chemokine CCL21, has been correlated with T cell infiltration and a positive prognosis in breast cancer and melanoma patients. However, the mechanisms controlling its development, and how it contributes to a beneficial outcome for cancer patients, are unknown. Here we demonstrate that LN-like PNAd+ CCL21+ vasculature develops in murine models of melanoma and lung carcinoma growing in multiple anatomic locations. PNAd expression on tumor-associated endothelium and CCL21 expression by tumor-associated endothelial cells and gp38+ fibroblasts was controlled by a novel mechanism dependent on tumor infiltrating effector lymphocytes that secreted LTα3. In intraperitoneal (IP) tumors, CCL21 was also controlled by IFNγ. While effector CD8 T cells induced LN-like vasculature in both subcutaneous (SC) and IP tumors, NK cells only promoted its development in SC tumors. In IP but not SC tumors, LN-like vasculature was associated with organized aggregates of B-lymphocytes and gp38+fibroblasts that resembled tertiary lymphoid organs. Importantly, this LN-like vasculature enabled the infiltration of adoptively transferred naïve T cells. These T cells underwent activation and effector cell differentiation in the tumor, and significantly delayed tumor outgrowth. These results establish LN-like vasculature as both a consequence of and key contributor to anti-tumor immunity.