Spontaneous fluctuations in brain activity are thought to underlie mind-wandering, moments when mental experience becomes unrelated to what one is currently doing. A large body of research has investigated ongoing neural oscillations in the alpha band (7–14 Hz), reflecting changes in arousal and attention. However, studies disagree whether the power of alpha oscillations increases or decreases during mind-wandering compared with on-task focus. We hypothesized that these opposite effects arise from differences in eye state across studies, as eye closure increases alpha power and can reverse alpha's relationship with sleepiness, which is itself related to mind-wandering. To test this, we recorded electroencephalography while male and female participants with eyes either open or closed were probed to report whether they were focused on the auditory attention task or mind-wandering and how alert or sleepy they were. Consistent with our hypothesis, we found that increased alpha power was more likely to precede mind-wandering and sleepiness in the eyes-open group but less likely in the eyes-closed group. A systematic literature review largely replicated these opposite relationships across eye states in different paradigms. We propose that these results reflect an inverted-U relationship between alpha power and mind-wandering, formed by a positive relationship at low alpha power values typical of eyes-open states and a negative relationship at high alpha power values typical of eyes-closed states. By sampling alpha power across eye states in the same paradigm, this work reconciles contradictions in prior literature and clarifies how ongoing neural oscillations reflect the stream of mental experiences.