Myeloid cells, including dendritic cells (DCs) and macrophages, are essential for establishing central tolerance in the thymus by promoting T cell clonal deletion and regulatory T cell (Treg) generation. Using single-cell transcriptomics and lineage-defining mouse models, we identified nine major populations of thymic myeloid cells with distinct lineage identities. What was previously considered a single "DC2" population is in fact composed of four distinct cell lineages: conventional DC2, monocyte-derived DCs (moDCs), monocyte-derived macrophages (moMacs), and a novel CX3CR1+ transitional DC (tDC) population. moDCs and moMacs depend on thymic IFN signaling to upregulate MHCII and CD11c, while conventional DC2 undergo intrathymic maturation through CD40 signaling. Among these populations, we have further characterized the tDC as a functionally distinct cell type with unique perivascular positioning and antigen surveillance capacity. tDCs reside in the perivascular space of thymic microvessels, are capable of taking up blood-borne antigens, and can present these antigens to developing T cells. Finally, we define the developmental origin and transcriptional dependencies that distinguish tDCs from all other known thymic myeloid populations. Together, these findings reveal the thymus as a niche for developmentally and functionally diverse myeloid cells and establish a role for thymic tDCs in blood-borne antigen sampling with direct implications for T cell selection.