The speed of visual search depends on bottom-up stimulus features (e.g., we quickly locate a red item among blue distractors), but it is also facilitated by the presence of top-down perceptual predictions about the item. Here, we identify the nature, source, and neuronal substrate of the predictions that speed up resumed visual search. Human subjects were presented with a visual search array that was repeated up to 4 times, while brain activity was recorded using magnetoencephalography (MEG). Behaviorally, we observed a bimodal reaction time distribution for resumed visual search, indicating that subjects were extraordinarily rapid on a proportion of trials. MEG data demonstrated that these rapid-response trials were associated with a prediction of (1) target location, as reflected by alpha-band (8–12 Hz) lateralization; and (2) target identity, as reflected by beta-band (15–30 Hz) lateralization. Moreover, we show that these predictions are likely generated in a network consisting of medial superior frontal cortex and right temporo-parietal junction. These findings underscore the importance and nature of perceptual hypotheses for efficient visual search.