Dendritic cells (DCs) bearing chemokine receptor CCR7 migrate from the tumor to the draining lymph node where they play a pivotal role in the induction of anti-tumor T cell responses. However, the similarities and differences in function and gene expression between DCs and other myeloid cell populations in the tumor remain unclear. Here, we analyzed the function and transcriptomic profile of tumor-infiltrating DCs using mouse subcutaneous tumor models. In the tumor, we identified a CCR7+ MHC class II+ cell population (CCR7+ tDCs) that expressed high levels of the DC-associated markers CD40 and CD205. Intra-tumoral injection of 100 kDa FITC-dextran revealed that CCR7+ DCs uptake macromolecules as efficiently as the CCR7- CD11b+ cell population. In addition, CCR7+ tDCs induced stronger antigen-specific T cell proliferation than other CCR7- tumor-infiltrating cell populations ex vivo. 3’ SAGE-seq analysis and subsequent WGCNA clustering analyses revealed that the gene expression profiles of CCR7+ tDCs more resembled CD326- migratory DCs in the dLN than CCR7- MHC class II+ cells in the tumor. Comparison of CCR7+ tDC-specific genes with a public dataset revealed that these genes are highly enriched in migratory DCs in the lymph nodes but not in monocytes, macrophages or resident type DCs. Collectively, our functional and transcriptional analyses suggest that CCR7+ tDCs are a precursor of migratory DCs in the dLN. Therapeutic strategies to augment the number and function of CCR7+ tDCs could be a useful strategy as part of combination tumor immunotherapy.