Age-related remodeling of the cardiac extracellular matrix (ECM) is a major contributor to cardiovascular disease and dysfunction. In aging, specific components of the ECM undergo abnormal secretion, degradation, structural changes, and mechanical alterations, directly affecting organ physiology and cell behavior. Specifically, the stiffness of murine cardiac tissue has been shown to increase from ~10 kPa (young) to ~40 kPa (aged), which has important implications in cellular mechanotransduction and function. While ECM stiffening often compensates for a weakening heart, these altered matrix properties can lead to further complications. It is well known that cardiac cells are mechanosensitive, but most current in vitro systems are incapable of decoupling distinct ECM cues while maintaining native scaffold properties. To do this, we developed a hybrid material approach termed DECIPHER (DECellularized In Situ Polyacrylamide Hydrogel-ECM hybRid) consisting of in situ decellularized ECM from intact cardiac tissue sections linked to a synthetic hydrogel. The ECM ‘ligand age’ can thus be tuned independently from the ECM ‘stiffness age’ via the manipulation of the synthetic hydrogel component connected to the tissue proteins, resulting in four scaffold combinations. DECIPHER scaffolds were used to elucidate the specific roles of these interconnected age-specific ECM cues (ligands vs. stiffness) in regulating cardiac fibroblast function. Scaffolds were first assessed using quantitative mass spectrometry, immunohistochemistry, and nanoindentation, and were found to maintain the original composition and organization of young or aged murine cardiac tissue while allowing independent control of the mechanical properties that reflect the stiffness of young (~10 kPa) or aged (~35 kPa) cardiac tissue. We then seeded these scaffolds with primary cardiac fibroblasts (CFs) isolated from young or aged murine hearts and carried out immunofluorescence, RNA-seq, and RT-qPCR. We discovered distinct age-dependent mechanisms of CF activation in which the integration of ligand and mechanical cues drive the phenotypical transition toward a myofibroblast state. Notably, for aged CFs, young ECM ligand presentation was found to outweigh profibrotic stiffness cues, thereby regulating CF quiescence and age phenotype independent of mechanics. Ultimately, these tunable scaffolds enable precise investigations into the specific properties of the ECM that regulate age-related dysfunction and provide insights into potential avenues for rejuvenation strategies.