Non‐Technical Summary  Oxidative stress is a hallmark of various cardiovascular disorders that results in cellular dysfunction and death. Reactive oxygen species (ROS)‐induced ROS release (RIRR) is a fundamental mechanism which amplifies ROS levels within the cardiomyocyte resulting in cellular oxidative stress. Despite elegant studies describing the phenomenon of RIRR in isolated myocytes, its biophysical properties and functional consequences in intact myocardium remain unclear. Here, we use ROS imaging to extend the concept of RIRR to the level of the intact heart. We establish regenerative superoxide production as the mediator of RIRR‐related arrhythmias and reveal their strong dependence on a key mitochondrial channel, known as the inner membrane anion channel (IMAC). We demonstrate the efficacy of suppressing RIRR and related arrhythmias either by pharmacologically blocking IMAC or scavenging ROS using a synthetic superoxide dismutase/catalase mimetic.