Despite the recognized contribution of environmental conditions in utero to childhood and adult disease, there is little data identifying which conditions during embryogenesis and which target tissues carry the epigenetic program that increases the susceptibility to insulin resistance (IR) in the offspring later in life. We demonstrated that specific VDR deletion was sufficient to induce IR, hypertension, and atherosclerosis by promoting proinflammatory macrophage infiltration of the vasculature and metabolic tissues. We found that induction of endoplasmic reticulum stress in mouse VDR null macrophages increases proinflammatory cytokines inducing IR and miR-106b-5p secretion, which stimulates juxtaglomerular cell renin production and hypertension via repression of transcription factors E2f1 and Pde3b. To determine whether vitamin D (VD) deficiency in utero programs embryonic hematopoietic immune cells (HSCs) to cause metabolic syndrome, we isolated fetal (E13) liver HSCs from embryos obtained from VD deficient or sufficient dams and transplanted into genotype-matched eight-week-old VD-sufficient mice. We found that recipients of fetal HSCs made VD deficient in utero-induced IR in VD-sufficient mice. VD deficiency epigenetically suppresses Jarid2 expression and activates the Mef2/PGC1a pathway in HSCs, which persists in recipient bone marrow, resulting in macrophage infiltration to adipose tissue. These macrophages secrete miR106-5p, which promotes adipose IR by repressing PIK3 catalytic and regulatory subunits and down-regulating AKT signaling. VD-deficient monocytes from human cord blood have comparable Jarid2/Mef2/PGC1a expression changes and secrete miR-106b-5p, causing adipocyte IR. These findings suggest that VD deficiency during development has epigenetic consequences on a single, non-metabolically active tissue compartment that is mitotically stable and sufficient to impact the systemic renin-angiotensin system and the metabolic milieu.