Abstract Body: Abdominal aortic aneurysm (AAA) formation and rupture reflect failure of vascular smooth muscle cell (VSMC) adaptation to chronic stress, yet the mechanisms governing adaptive versus maladaptive remodeling of the aortic wall remain poorly defined. Myocardin (MYOCD) is traditionally viewed as a master regulator of the VSMC contractile phenotype and is broadly assumed to be protective in aneurysm disease. Challenging this paradigm, we demonstrate that VSMC-specific MYOCD deficiency completely prevents angiotensin II–induced AAA formation and markedly reduces rupture susceptibility, whereas VSMC-specific Myocd transgenic mice exhibit exacerbated aneurysm severity and increased rupture risk. Using integrated genetic models, chromatin occupancy analyses, bulk transcriptomics, and single-nucleus multiomic profiling, we redefine MYOCD as a central regulator of VSMC functional remodeling rather than a simple enforcer of contractile identity. Mechanistically, MYOCD directly transactivates ASB2, a proteostasis regulator, through the SRF/CArG-dependent pathway, establishing a transcriptional link to proteostatic control. Single-nucleus multiome analyses revealed that MYOCD deficiency does not merely suppress contractile programs but instead promotes adaptive VSMC state transitions, characterized by expansion of resilience-associated smooth muscle cell clusters and coordinated dampening of ubiquitin–proteasome and autophagy–lysosome pathways. Consistent with this model, siRNA-mediated ASB2 silencing functionally rescued MYOCD-driven proteostatic remodeling by attenuating autophagy–lysosome–dependent collagen 1 degradation, establishing ASB2 as a necessary downstream effector of MYOCD-mediated extracellular matrix turnover. Together, these findings establish a new conceptual framework in which MYOCD orchestrates VSMC functional gene programs beyond contractile differentiation. They further suggest that therapeutic benefit may be best achieved by redirecting stress-driven VSMC state transitions toward adaptive, resilience-associated phenotypes rather than enforcing contractile identity.