Aortic stiffness is a risk factor for hypertension and a major contributor to cardiovascular disease. Despite its clinical significance, the spatially distinct mechanisms driving vascular remodeling across the arterial wall remain poorly understood. Previous transcriptomic studies of the aorta do not distinguish between arterial layers, limiting our understanding of how layer-specific cell populations contribute to vascular remodeling. Here, we demonstrate a spatially resolved single-cell ribonucleic acid-sequencing (scRNA-seq) atlas of the aorta in response to 4 weeks of Angiotensin II (Ang II), with or without voluntary wheel running (EX), an intervention known to reduce aortic stiffness. We separately profiled the transcriptional landscapes of the intima–media (I+M) and adventitia layers across four experimental groups. Ang II induced a distinct layer-specific immune landscape, characterized by an expansion of cytotoxic T cells and Trem2⁺ macrophages in the intima–media (I+M), and increased cytotoxic T cells and inflammatory monocyte-derived macrophages in the adventitia. Ang II induced phenotypic remodeling of vascular smooth muscle cells (VSMCs), promoting a transition from homeostatic/contractile state to the modulated phenotype. This shift was accompanied by an increase in profibrotic fibroblast clusters enriched for extracellular matrix (ECM)-related genes in the adventitia. Exercise attenuated these changes by promoting an inflammation resolving VSMC phenotype and enhancing reparative fibroblasts. Additionally, RNA velocity analysis revealed divergent trajectories for VSMCs and fibroblasts in disease versus exercise conditions. Cell–cell communication analysis revealed that Ang II enhances intercellular interactions, particularly among immune cells and between immune cells and vascular cells, including VSMCs and fibroblasts, contributing to a pro-inflammatory and vascular remodeling. Exercise attenuated these interactions, indicating a shift toward vascular quiescence. Notably, Tnf–Tnfrsf1a interactions emerged as a central communication mediating immune cell–immune cell and immune cell– VSMCs/fibroblasts crosstalk, which was activated by Ang II and suppressed by exercise. This study provides the first anatomically stratified single-cell atlas of the aorta in hypertension and identifies key immune–vascular interactions that drive aortic stiffness. These findings offer mechanistic insight into how exercise restores vascular homeostasis and suggest potential therapeutic targets to counteract arterial remodeling.