Our objective was to demonstrate that human right-handedness, is not species specific, precipitated from language areas in the brain, but rather is context specific and inherited from a behavior common to both humans and great apes. In general, previous methods of assessing human handedness have neglected to consider the context of action or employed methods suitable for direct comparison across species. We employed a bottom-up, context-sensitive method to quantitatively assess manual actions in right-handed, typically developing children during naturalistic behavior. By classifying the target to which participants directed their manual action, as animate (social partner, self) and inanimate (non-living functional objects), we found that children demonstrated a significant right-hand bias for manual actions directed towards inanimate targets, but not for manual actions directed towards animate targets. This pattern was Comparisons of handedness patters support the view that human handedness, and its origin in cerebral lateralization is not a new or human-unique characteristic. Additionally these data are consistent with the theory that human population-level right-handedness is a trait developed through tool use that was inherited from an ancestor common to both humans and great apes.