A male advantage in spatial abilities is predicted to evolve in species where males rely on expansion of home territory to locate dispersed mates during the breeding season. We sought to examine mechanistic underpinnings of this evolved trait by comparing spatial navigational abilities in two species of Peromyscus that employ widely different reproductive strategies. Males and females from outbred stocks of deer mice (P. maniculatus bairdii) in which males engage in territorial expansion and mate search and California mice (P. californicus insignis), in which males do not, were administered tasks that assessed spatial learning and memory, and activity and exploratory behaviours. The maze employed for these studies included four spatial cues that could be used to aid in locating 1 of 12 potential escape holes. As predicted, male deer mice outperformed conspecific females and California mice males in maze performance and memory, and this difference appeared to be due to extent to which animals used spatial cues to guide maze navigation. Consistent with territorial expansion as a component of competition for mates, male deer mice were more active and engaged in more exploratory and less anxiety-related behaviours than conspecific females and California mice males. The results have implications for understanding and studying the cognitive and behavioural mechanisms that have evolved through male-male competition that involves territorial expansion and mate search.