Sex differences in spatial cognition are well documented; males typically outperform females on tasks dealing with mental rotation and spatial navigation, while females tend to outperform males on tasks dealing with object location, relational object location memory, or spatial working memory. Here we investigated both behavioral and neural sex differences in sex-specific spatial abilities. In Experiment 1, sixty-six (30 males, 36 females) participants completed computerized mental rotation (MR) and spatial working memory (SWM) tasks. In Experiment 2, twelve (6 males, 6 females) participants were given slightly modified versions of the same tasks during functional magnetic resonance imaging (fMRI). In both experiments, males outperformed females on the MR task, but no behavioral sex difference was observed on the SWM task. Males showed more activation in left parahippocampal gyrus, right medial frontal gyrus, inferior parietal lobe, inferior frontal gyrus in the MR task. Females showed activation in the left parahippocampal gyrus only. For the study condition of the spatial working memory task, females showed activation in left inferior frontal gyrus, while males activated left inferior parietal and medial frontal areas. In the test conditions, females showed activation in the right inferior frontal gyrus, left middle temporal gyrus, and left parahippocampal gyrus. Males activated right medial frontal gyrus and inferior parietal lobe. Interestingly, similar regions – parahippocampal gyrus, inferior parietal lobe, and middle temporal gyrus - were found to be active when males solved mental rotation tasks and females solved spatial working memory tasks. Further, performance was modulated by activation in the parahippocampal gyrus and middle temporal gyrus for males and the middle temporal gyrus and inferior frontal gyrus for females. These data extend previous claims for sex differences in sex specific spatial cognitive abilities by demonstrating both behavioral and neural sex differences consistent with an evolutionary model, which suggests sexual selection may have favored sex-differences in such abilities and the neural substrates that sub-serve those processes.