Widespread religious disbelief represents a key testing ground for theories of religion. We evaluated the predictions of three prominent theoretical approaches in a nationally representative (USA, N= 1417) dataset with preregistered analyses, and found considerable support for a dual inheritance (gene-culture coevolution) perspective. We found that witnessing fewer credible cultural cues of religious commitment is the most potent predictor of religious disbelief, β=0.28, followed distantly by reflective cognitive style, β= 0.13, and less advanced mentalizing, β= 0.05. Low cultural exposure to faith predicted about 90% higher odds of atheism than did peak cognitive reflection. Further, cognitive reflection predicted reduced religious belief only among individuals who witness relatively fewer credible contextual cues of faith in others. This work empirically unites four distinct literatures addressing the origins of religious disbelief, highlights the utility of considering both evolved intuitions and cultural evolutionary processes in religious transmission, emphasizes the dual roles of content- and context-biased social learning, and sheds light on the shared psychological mechanisms that underpin both religious belief and disbelief.