The cellular and molecular mechanisms underlying tumor cell PD-L1 (tPD-L1) function in tumor immune evasion are incompletely understood. We report here that tPD-L1 does not suppress cytotoxic T lymphocyte (CTL) activity in co-cultures of tumor cells and tumor-specific CTLs and exhibits no effect on primary tumor growth. However, deleting tPD-L1 decreases lung metastasis in a CTL-dependent manner in tumor-bearing mice. Depletion of myeloid cells or knocking out PD-1 in myeloid cells (mPD-1) impairs tPD-L1 promotion of tumor lung metastasis in mice. Single-cell RNA sequencing (scRNA-seq) reveals that tPD-L1 engages mPD-1 to activate SHP2 to antagonize the type I interferon (IFN-I) and STAT1 pathway to repress Cxcl9 and impair CTL recruitment to lung metastases. Human cancer patient response to PD-1 blockade immunotherapy correlates with IFN-I response in myeloid cells. Our findings determine that tPD-L1 engages mPD-1 to activate SHP2 to suppress the IFN-I-STAT1-CXCL9 pathway to impair CTL tumor recruitment in lung metastasis. [Display omitted] • Tumor PD-L1 (tPD-L1) does not suppress CTL cytotoxicity in vitro • TPD-L1 promotes metastatic, but not primary, tumor growth via a CTL-dependent mechanism • TPD-L1 engages myeloid PD-1 (mPD-1) to repress IFN-I to impair CTL tumor recruitment • Human patient response to nivolumab correlates with IFN-I response in myeloid cells Klement et al. use single-cell RNA-seq, PD-L1/PD-1-deficient cell lines, and mouse tumor models to elucidate the cellular and molecular mechanism underlying tumor cell PD-L1 function in tumor immune evasion. They find that tumor cell PD-L1 does not promote tumor immune evasion in the primary tumor site but engages myeloid cell PD-1 to activate SHP2 to antagonize the IFN-I-STAT1-CXCL9 intrinsic pathway in myeloid cells to suppress T cell recruitment in lung metastases. [ABSTRACT FROM AUTHOR]