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The mechanisms shaping their diverse functions in the tumors remain poorly understood and may offer therapeutic opportunities. Here, we identify the lipid-presenting molecule CD1d as a regulator of tumor progression and myeloid heterogeneity in the tumor microenvironment. Using several mouse models of breast cancer, we demonstrate that genetic deletion or antibody-mediated targeting of CD1d leads to reduced tumor growth, altered immune infiltration, and improved efficacy of anti-PD-1 immunotherapy. Specifically, CD1d targeting reshapes the intratumoral myeloid compartment, enhancing proinflammatory programs and resulting in accumulation of inflammatory monocytes. The CD1d-dependent control of myeloid cell functional differentiation is cell-intrinsic and conserved in human and mouse. Through single-cell RNA sequencing, we define the transcriptional landscape associated with CD1d deficiency and derive a gene signature that correlates with clinical outcomes and response to immunotherapy in breast cancer patients. 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