Conventional dendritic cells (cDCs) are traditionally subdivided into cDC1 and cDC2 lineages, each characterised by specialised functions to shape T cell responses as required. Using imaging flow cytometry, we observed a population of DCs co-expressing cDC1 and cDC2-associated surface molecules. Using single-cell RNA sequencing with integrated cell surface protein expression (CITE-seq), we found that a proportion of mature cDC1 cells co-expressed cDC2 characteristic surface features, and a population of Sox4 and Siglech expressing DCs co-expressed features traditionally associated with cDC1, cDC2, pDCs and monocytes. We observed that mice lacking the cDC1-required transcription factor Batf3 harboured increased numbers of DCs with lineage-mixed features. Here, mitotic immature Batf3-/- cDC1-like cells showed reduced expression of cDC1 features and increased levels of cDC2 features. An optimized flow cytometry panel allowed validation of these CITE-seq derived DC cell states. In conclusion, these data suggest that multiple cDC cell states can co-express lineage-overlapping features, revealing a level of previously unappreciated phenotypic cDC plasticity.