This study reports an analysis of 20 T1-weighted MRI scans from tufted capuchin monkeys (5 male, 15 female). We carried out a data-driven, whole-brain volumetric analysis on regional gray matter anatomy using voxel-based morphometry. This revealed that males showed statistically significant expansion of a region of the hypothalamus, while females showed significant expansion in a distributed set of regions, including the cerebellum, early visual cortex, and higher-order visual regions spanning occipital and temporal cortex. In order to elucidate the network connectivity of these regions, we employed probabilistic tractography on diffusion tensor imaging data. This showed that the female-enlarged regions connect with distributed association networks across the brain. Notably, this contrasts with rodent studies, where sex differences are focused in deep, ancestral limbic regions involved in the control of reproductive behavior. Additionally, in our dataset, for several regions, male and female volumetric measures were completely non-overlapping. This contrasts with human studies, where sex differences in cortical regions have been reported, but are characterized by overlapping rather than divergent male and female values. We suggest that these results can be understood in the context of the different lifetime experiences of males and females, which may produce increased experience-dependent cortical plasticity in capuchins compared to rodents, and in humans compared to capuchins.