Infiltration of regulatory T (Treg) cells, an immunosuppressive population of CD4+ T cells, into solid cancers represents a barrier to cancer immunotherapy. Chemokine receptors are critical for Treg cell recruitment and cell-cell interactions in inflamed tissues, including cancer, and thus are an ideal therapeutic target. Here, we show in multiple cancer models that CXCR3+ Treg cells were increased in tumors compared with lymphoid tissues, exhibited an activated phenotype, and interacted preferentially with CXCL9-producing BATF3+ dendritic cells (DCs). Genetic ablation of CXCR3 in Treg cells disrupted DC1-Treg cell interactions and concomitantly increased DC-CD8+ T cell interactions. Mechanistically, CXCR3 ablation in Treg cells increased tumor antigen-specific cross-presentation by DC1s, increasing CD8+ T cell priming and reactivation in tumors. This ultimately impaired tumor progression, especially in combination with anti-PD-1 checkpoint blockade immunotherapy. Overall, CXCR3 is shown to be a critical chemokine receptor for Treg cell accumulation and immune suppression in tumors. Display omitted •CXCR3 is elevated on Treg cells within draining lymph nodes and tumors•CXCR3+ Treg cells co-localize with CXCL9-producing type 1 DCs in tumors•Disrupting CXCR3 in Tregs increases tumor antigen cross-presentation by DC1s in tumors•Loss of CXCR3 in Treg cells boosts tumor CD8+ T cells and slows cancer progression Regulatory T (Treg) cell accumulation in tumors suppresses antitumor immunity, but the mechanisms are incompletely understood. Here, Moreno Ayala et al. show that CXCR3 expression on Treg cells puts them in close proximity to CXCL9-producing dendritic cells in tumors, where they suppress tumor antigen presentation and impede the antitumor CD8+ T cell response.