CX₃CR1 expression is associated with the commitment of CSF-1R⁺ myeloid precursors to the macrophage/dendritic cell (DC) lineage. However, the relationship of the CSF-1R⁺ CX₃CR1⁺ macrophage/DC precursor (MDP) with other DC precursors and the role of CX₃CR1 in macrophage and DC development remain unclear. We show that MDPs give rise to conventional DCs (cDCs), plasmacytoid DCs (PDCs), and monocytes, including Gr1⁺ inflammatory monocytes that differentiate into TipDCs during infection. CX₃CR1 deficiency selectively impairs the recruitment of blood Gr1⁺ monocytes in the spleen after transfer and during acute Listeria monocytogenes infection but does not affect the development of monocytes, cDCs, and PDCs.