Dendritic cells play a vital role in antitumor immunity by acquiring antigens in the tumor microenvironment and transporting them to tumor-draining lymph nodes (tDLNs) to prime T cell responses. However, factors within the TME that regulate DC functional state and trafficking remain incompletely understood. Here, we investigated how targeting a tumor-derived chemokine shapes DC function, migration, and antigen transport, particularly for the cDC1 subset, between tumors and tDLNs. Carcinogen-induced tumor (CIT) squamous cell carcinoma cell lines were used to model immune-cold tumors in mice. Multiplex ELISAs revealed high CX3CL1 expression in tumor lysates, and CRISPR-Cas9-mediated deletion of CX3CL1 in these cold cell lines transformed the cold tumor phenotype, with low T and DC infiltration, into an immune-hot phenotype with high infiltration, suggesting CX3CL1's dominant influence on the TME. In addition to local effects of CX3CL1 on the TME, we examined its systemic impact on the immune cell composition of other lymphoid organs in tumor-bearing mice during early- and mid-stage tumor development. We identified a higher prevalence of DCs, particularly cDC1, in the tDLNs of CX3CL1^low tumors than in parental tumors. Moreover, these cDC1 populations in knockout tumors expressed antigen-presenting marker (CD103), migratory marker (CCR7), co-stimulatory markers (CD83, CD86), and maturation marker (CD40) in the tumors and tDLNs, more than in the parental counterpart. These results were further confirmed in vitro using bone marrow-derived DCs treated with or without CX3CL1-enriched supernatant. To further confirm the antigen-presenting capacity of DCs, we used a confetti mouse cassette to generate RFP-colored CX3CL1^Hi and CX3CL1l^ow tumors. We observed a higher proportion of cDC1 cells carrying RFP in CX3CL1^low tumors and tDLNs than in parental tumors. These data identify a tumor-derived chemokine as a key regulator of cDC1 functional state and tumor–tDLN coordination, highlighting a strategy cold tumors adopt to evade DC-mediated anti-tumor immunity.