Aging is the predominant risk factor for atherosclerosis, the leading cause of death. Rare smooth muscle cells (SMCs) clonally expand giving rise to up to ∼70\% of atherosclerotic plaque cells; however, the effect of age on SMC clonality is not known. Our results indicate that aging induces SMC polyclonality and worsens atherosclerosis through non-cell autonomous effects of aged bone marrow-derived cells. Indeed, in myeloid cells from aged mice and humans, TET2 levels are reduced which epigenetically silences integrin β3 resulting in increased cytokine (e.g., tumor necrosis factor [TNF]-α) signaling. In turn, TNFα induces recruitment and expansion of multiple SMCs into the atherosclerotic plaque. Recent studies demonstrate that normal aging is characterized by somatic mutations and clonal expansion of epithelial cells of diverse tissues (e.g., esophagus, endometrium, skin); extrapolating beyond atherogenesis, our results call for future studies evaluating the role of aged myeloid cells in regulating this epithelial cell clonal expansion.