Transitional dendritic cells (tDCs) share phenotypic and transcriptional features of plasmacytoid DCs (pDCs) and type 2 DCs (DC2s). Studies of tDCs have primarily focused on human blood and mouse spleen, leaving tDC distribution and phenotypic characteristics in peripheral tissues incompletely defined. As previously described, healthy skin lacks pDCs and tDCs with the phenotypes observed in lymphoid organs. However, skin harbors a population of DC2s that lacks CD11b and closely resembles the splenic tDC-derived CD11b⁻ DC2s previously described by our group. These cells are also present in the migratory compartment of skin-draining lymph nodes (sLNs). Several lines of evidence support a tDC origin for skin and migratory CD11b⁻ DC2s. First, skin CD11b⁻ DC2s express TCF4, a transcription factor that maintains pDC and tDC identity, whereas its expression decreases in their migratory counterparts in sLNs. Second, CD11b⁻ DC2s in both skin and sLNs are lost following conditional Tcf4 deletion or depletion of pDC/tDC progenitors (pro-pDCs). Finally, intradermal adoptive transfer of splenic tDCs generates migratory CD11b⁻ DC2s in sLNs. These findings support a tDC origin for skin CD11b⁻ DC2s and their migratory counterparts in sLNs. Together, our results extend the contribution of the pDC/tDC lineage beyond lymphoid organs and identify it as a previously unrecognized source of DC2 heterogeneity in peripheral tissues.