The adaptive gain theory highlights the pivotal role of the locus coeruleus–noradrenergic (LC-NE) system in regulating task engagement. In humans, however, LC-NE functional dynamics remain largely unknown. We evaluated the utility of two candidate psychophysiological markers of LC-NE activity: the P3 event-related potential and pupil diameter. Electroencephalogram and pupillometry data were collected from 24 participants who performed a 37-min auditory oddball task. As predicted by the adaptive gain theory, prestimulus pupil diameter exhibited an inverted U-shaped relationship to P3 and task performance such that largest P3 amplitudes and optimal performance occurred at the same intermediate level of pupil diameter. Large phasic pupil dilations, by contrast, were elicited during periods of poor performance and were followed by reengagement in the task and increased P3 amplitudes. These results support recent proposals that pupil diameter and the P3 are sensitive to LC-NE mode.