Noninvasive studies of speed-accuracy tradeoff (SAT) highlight contributions of medial frontal cortex (MFC), but its role is disputed. Hence, neural spiking was sampled in supplementary eye field (SEF) of MFC and in visuomotor frontal eye field (FEF) and superior colliculus (SC) in macaques performing an SAT task. Like visuomotor structures, SEF neurons signaled proactive urgency and stimulus salience when SAT cues changed. Unlike visuomotor structures, SEF modulation signaled choice and timing errors, which predicted production of corrective saccades and signaled reward prediction error. Simultaneous spiking sampled in SEF and visuomotor structures revealed quantitative but not qualitative modulation across SAT states with stronger correlations following errors. These results contextualize findings using noninvasive measures, complement neurophysiological findings in visuomotor structures, endorse the role of medial frontal cortex as a critic for the actor instantiated in visuomotor structures, and improve our understanding of the distributed neural mechanisms of SAT.