Unrelated males sometimes share their nests and their mates, an example of male-male cooperation that calls for an evolutionary explanation. We developed a game-theoretic model of this situation under the assumption that males could be either “aggressors,” attempting to drive off any other arriving male, or “tolerators,” willing to share a nest and mates with another tolerator male. We modeled nest dynamics by changing the frequency of the two types in the population and determined how this affected their fitness. We use the sea lamprey as a case study to generate a plausible array of behavioral traits and ecological conditions for the model. Under these conditions, only aggressors or only tolerators could persist, not both, but we also show how exceptions can arise. Aggressors predominated for the standard conditions we chose, but tolerators could take over when females favored them through nest choice or increased mating rate. High nesting densities and high fighting costs also tended to favor tolerators. At moderate to low densities of individuals in the nesting area, female behavior, based on their own costs and benefits, should determine the outcome.