An emerging body of work has demonstrated that resting-state non-oscillatory, or aperiodic, 1/f neural activity is a functional and behaviorally relevant marker of cognitive function capacity. In the motor domain, previous work has only applied 1/f analyses to investigations of motor coordination and performance measures. The value of aperiodic resting-state neural dynamics as a marker of individual visuomotor performance capacity remains unknown. Accordingly, the aim of this work was to investigate if individual 1/f intercept and slope parameters of aperiodic resting-state neural activity predict reaction time and perceptual sensitivity in an immersive virtual reality marksmanship task. The marksmanship task required speeded selection of target stimuli and avoidance of selecting non-target stimuli. Motor and perceptual demands were incrementally increased across task blocks and participants performed the task across three training sessions spanning one week. When motor demands were high, steeper individual 1/f slope predicted shorter reaction time. This relationship did not change with practice. Increased 1/f intercept and a steeper 1/f slope were associated with higher perceptual sensitivity, measured as d'. However, this association was only observed under the highest levels of perceptual demand and only in the initial exposure to these conditions. Individuals with a lower 1/f intercept and a shallower 1/f slope demonstrated the greatest gains in perceptual sensitivity from task practice. These findings demonstrate that individual differences in motor and perceptual performance can be accounted for with resting-state aperiodic neural dynamics. The 1/f aperiodic parameters are most informative in predicting visuomotor performance under complex and demanding task conditions. In addition to predicting capacity for high visuomotor performance with a novel task, 1/f aperiodic parameters might also be useful in predicting which individuals might derive the most improvements from practice.