Opportunistic actors — who behave expediently, cheating when they can and offering minimal cooperation only when they have to — play an important role in producing some puzzling phenomena, including the flourishing of strong reciprocity, the peculiar correlation between positive and negative reciprocity within cultures of honor, and low levels of social capital within tight and collectivist cultures (that one might naively assume would produce high levels of social capital). Using agent-based models and an experiment, we show how Opportunistic actors enable the growth of Strong Reciprocators, whose strategy is the exact opposite of the Opportunists. Additionally, previous research has shown how the threat of punishment can sustain cooperation within a group. However, the present studies illustrate how stringent demands for cooperation and severe punishments for noncooperation can also backfire and reduce the amount of voluntary, uncoerced cooperation in a society. The studies illuminate the role Opportunists play in producing these backfire effects. In addition to highlighting other features shaping culture (e.g., risk and reward in the environment, “founder effects” requiring a critical mass of certain strategies at a culture’s initial stage), the studies help illustrate how Opportunists create aspects of culture that otherwise seem paradoxical, are dismissed as “error,” or produce unintended consequences.