Visual processing can be facilitated by covert attention at behaviorally relevant locations. If the eyes move while a location in the visual field is facilitated, what happens to the internal representation of the attended location? With each eye movement, the retinotopic (eye-centered) coordinates of the attended location change while the spatiotopic (world-centered) coordinates remain stable. To investigate whether the neural substrates of spatial attention reside in retinotopically and/or spatiotopically organized maps, we used a novel gaze-contingent behavioral paradigm that probed spatial attention at various times after eye movements. When task demands required maintaining a spatiotopic representation after the eye movement, we found facilitation at the retinotopic location of the spatial cue for 100-200 ms after the saccade, although this location had no behavioral significance. This task-irrelevant retinotopic representation dominated immediately after the saccade, whereas at later delays, the task-relevant spatiotopic representation prevailed. However, when task demands required maintaining the cue in retinotopic coordinates, a strong retinotopic benefit persisted long after the saccade, and there was no evidence of spatiotopic facilitation. These data suggest that the cortical and subcortical substrates of spatial attention primarily reside in retinotopically organized maps that must be dynamically updated to compensate for eye movements when behavioral demands require a spatiotopic representation of attention. Our conclusion is that the visual system's native or low-level representation of endogenously maintained spatial attention is retinotopic, and remapping of attention to spatiotopic coordinates occurs slowly and only when behaviorally necessary.