Categorical versus coordinate spatial tasks rely differentially on the left versus right hemisphere. Given the neuroanatomical and neurophysiological differences between inconsistent- versus consistent-right-handers (ICH versus CRH, respectively), such that the former demonstrates increased access to right hemisphere processes relative to the latter, it was hypothesized that ICH would outperform CRH on a test of coordinate spatial knowledge. Previous work demonstrating reliance on the right hemisphere for both categorical and coordinate information in non-right-handers using lateralized stimuli of brief duration suggested ICH might also outperform CRH on a categorical task as well. Participants navigated a virtual environment, landmark-to-landmark, within a 3-dimensional first-person point of view with high ecological validity, and then were tested on either their categorical or coordinate spatial knowledge. ICH were superior relative to the CRH on both types of spatial knowledge. Additionally, ICH navigated the environment during learning more quickly, and reported being more confident in their knowledge of the location of landmarks within the environment, compared with CRH. Results are discussed in terms of potential handedness differences in spatial ability generally