Conventional dendritic cells (cDCs) comprise functionally and phenotypically diverse populations, including cDC1s and cDC2s. The latter population has been variously sub-divided into NOTCH-dependent cDC2s, KLF4-dependent cDC2s, T-bet+ cDC2As and T-bet– cDC2Bs, but it is unclear how all these sub-types are interrelated and to what degree they represent cell states or cell subsets. All cDCs derive from bone marrow progenitors called pre-cDCs, that circulate through the blood to colonise peripheral tissues. Here, we identifed distinct mouse pre-cDC2 subsets biased to give rise to cDC2As or cDC2Bs. We showed that a SiglecH+ pre-cDC2A population in the bone marrow preferentially gave rise to SiglecH- CD8α+ pre-cDC2As in tissues, which differentiated into T-bet+ cDC2As. In contrast, a SiglecH- fraction of pre-cDCs in the bone marrow and periphery mostly generated T-bet– cDC2Bs, a lineage marked by expression of LYSM. Our results showed that cDC2A vs cDC2B fate specification started in the bone marrow and suggest that cDC2 subsets were ontogenetically-determined lineages, rather than cell states imposed by the peripheral tissue environment.