There are two major myeloid pulmonary dendritic cell (DC) populations: CD103+ DCs and CD11b high DCs. In this study, we investigated in detail the origins of both myeloid DC pools using multiple experimental approaches. We show that, in resting lung, Ly-6C high CCR2 high monocytes repopulated CD103+ DCs using a CCR2-dependent mechanism, and these DCs preferentially retained residual CCR2 in the lung, whereas, conversely, Ly-6C low CCR2 low monocytes repopulated CD11b high DCs. CX3CR1 was required to generate normal numbers of pulmonary CD11b high DCs, possibly because Ly-6C low monocytes in the circulation, which normally express high levels of CX3CR1, failed to express bcl-2 and may have diminished survival in the circulation in the absence of CX3CR1. Overall, these data demonstrate that the two circulating subsets of monocytes give rise to distinct tissue DC populations.