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Attention can be shifted within internal representations maintained in working memory. These retroactive processes are particularly inherent to the processing of auditory information that is especially transient over time and thus, requires us to continuously maintain, attend to, and integrate information in working memory. Using EEG recordings, the present study investigated the neurophysiological mechanisms underlying selective spatial attention in a retroactive as opposed to a perceptual auditory search task. Two kinds of sound stimuli were employed: a horizontal sound array consisting of two natural sounds presented simultaneously in the left and right hemispace and a central single target sound. The target sound was provided either after (retroactive search) or before the presentation of the sound array (perceptual search). In both search conditions, participants completed a sound localization and a sound detection task, indicating the position (left or right) or the presence versus absence (yes or no) of a particular target sound. Analyses revealed a lateralization of alpha power oscillations (8–12Hz) over parieto-occipital scalp in both perceptual and retroactive sound localization tasks, but not in respective sound detection tasks, suggesting auditory alpha lateralization to be restricted to spatially-specific task demands. The observed asymmetric modulations of alpha power in sound localization are consistent with analogous findings from the visual domain, supporting the supramodal role of alpha oscillations in the deployment of spatial attention. Hence, we conclude that auditory alpha lateralization is a higher-order attention mechanism that operates in perceptual and mnemonic space reflecting the access to a spatially-specific, supramodal response template.