Solid tumors contain large numbers of inflammatory cells, including monocytes and monocyte-derived macrophages, which are involved in both pro- and anti-tumor immune responses. During tumor development, the bone marrow dramatically accelerates production of monocytes, rapidly transferring many of these newly formed cells to a reservoir in the spleen [Shand et al., PNAS 111:7771 (2014)]. However, due to an intrinsic difference in migration potential, BM monocytes are 2.7 times more likely to migrate into the tumor from the circulation than spleen monocytes. In fluorescent ubiquitination-based cell-cycle indicator (Fucci) mice, the Fucci-red fusion protein undergoes proteolysis during the S/G2/M phases of the cell cycle but accumulates during the G1 phase, thus providing an indication of the time elapsed since last cell division. Because BM monocytes were younger than those in the spleen, we hypothesized that monocyte phenotype and migration potential changes depending on their level of maturity. Here, we characterized monocyte development in Fucci mice bearing LLC subcutaneous tumors, EO771.LMB orthotopic tumors implanted in the mammary fat pad, and tumors that develop spontaneously in the mammary fat pads of MMTV-PyVT-Fucci mice. As peripheral blood monocytes aged, we observed downregulation of Ly-6C, consistent with the transition of these cells from an inflammatory to patrolling phenotype. However, even within the Ly-6Chi inflammatory monocyte population, CCR2 and CX3CR1 expression decreased as cells matured. After entering the tumor, maturation correlated with an increase in MHC class II expression, consistent with the differentiation of these cells into inflammatory macrophages. Because CCR2 plays a crucial role in the recruitment of tumor-infiltrating monocytes, these results provide an explanation for the preferential recruitment of younger BM-derived monocytes to the tumor. By identifying points of control of monocyte development in healthy and tumor-bearing mice, our results may identify novel ways to modulate the supply of monocytes and macrophages to the tumor.