Growing evidence demonstrates that alpha-band (8–12 Hz) oscillations play an important role in spatial attention and working memory (WM). Here we combined electroencephalography (EEG) with an inverted spatial encoding model to examine whether the topography of alpha-band oscillations across the scalp tracks the specific spatial locations held in WM. Across three experiments, human participants performed spatial delayed-estimation tasks in which they remembered the precise angular location of a stimulus across a delay period and then reproduced that location on a continuous ring. Applying an inverted spatial encoding model to the scalp distribution of EEG power revealed that although low-frequency power transiently tracked stimulus location immediately following stimulus onset across multiple frequency bands, only total alpha-band power persistently tracked the specific spatial location held in WM throughout the retention interval. Reconstructed channel-tuning functions in the alpha band were finely tuned to the remembered location, tracked the prioritized location following a retrospective cue, and were eliminated when spatial storage was not required. These findings demonstrate that the topography of scalp alpha-band activity directly tracks the content of spatial working memory.