Dilated Cardiomyopathy (DCM) is a major cause of cardiac death which can arise via various mutations in the contractile proteins of the cardiomyocyte. In order to explore subcellular mechanisms of this disease and a potential treatment called 2-deoxy-ATP (dATP), we employ multiscale modeling from the atomistic to cellular level. We use molecular dynamics (MD) and Brownian dynamics (BD) studies to explore the effects of 3 major DCM-associated mutations (D75Y,E59D, and G159D) on cardiac troponin C, and integrate simulation-gathered transition rates into a Markov State model (MSM) of the sarcomere to predict cellular contractile effects. We employ BD simulations to probe the electrostatic affinity of tropomyosin as it rotates about the actin thin filament, developing a multi-well energy landscape which can be used in higher-order stochastic models of sarcomere activation. Using BD, we discover that dATP-bound myosin has increased affinity to an actin dimer compared to ATP-myosin, indicating that dATP treatment enhances crossbridge (XB) attachment rates. Integrating this information into a Monte Carlo MSM of crossbridge cycling, we quantify the effect of dATP treatment on XB attachment, powerstroke and detachment rates which explain augmented force development and magnitude in both steady-state and twitch simulations. Finally, we investigate the effects of dATP on calcium handling through Gaussian accelerated MD on apo, Mg.ATP-bound, and Mg.dATP-bound SR-ATPase (SERCA 2A) to determine effects of the drug on protein conformation. BD is employed to measure ATP- vs dATP- association rates as well as Ca2+ binding rates. We found that dATP has higher affinity for SERCA 2A than ATP, and when dATP is bound Ca2+ prefers to bind calcium Site II rather than Site I, in direct opposition to the ATP case. We found that these two rate differences can partially explain experimentally noted effects of dATP on the calcium transient when scaled up to an ODE model of calcium handling, but we can fully explain the effects by altering other rates in the SERCA cycle and analyzing other Ca2+-ATPases. These studies provide pipelines for the integration of computational technologies at multiple spatial and temporal scales to answer biophysical questions about DCM mechanisms and treatments.