Although previous research with human and nonhuman primates has examined the neural correlates of performance monitoring, discrepancies in methodology have limited our ability to make cross-species generalizations. One major obstacle arises from the use of different behavioral responses and tasks across different primate species. Specifically, it is unknown whether performance-monitoring mechanisms rely on different neural circuitry in tasks requiring oculomotor vs. skeletomotor responses. Here, we show that the human error-related negativity (ERN) elicited by a saccadic eye-movement response relative to a manual response differs in several critical ways. The human saccadic ERN exhibits a prolonged duration, a broader frontomedial voltage distribution, and different neural source estimates than the manual ERN in exactly the same stop-signal task. The human saccadic error positivity (Pe) exhibited a frontomedial voltage distribution with estimated electrical sources in supplementary motor area and rostral anterior cingulate cortex for saccadic responses, whereas the manual Pe showed a posterior scalp distribution and potential origins in the superior parietal lobule. These findings constrain models of the cognitive mechanisms indexed by the ERN/Pe complex. Moreover, by paralleling work with nonhuman primates performing the same saccadic stop-signal task (Godlove et al. 2011), we demonstrate a cross-species homology of error event-related potentials (ERPs) and lay the groundwork for definitively localizing the neural sources of performance-monitoring ERPs.