We developed a new experimental task to investigate the relative timing of neural activity during shifts of spatial attention with event-related potentials. The task enabled the investigation of nonlateralized as well as lateralized neural activity associated with spatial shifts. Participants detected target stimuli within one of two peripheral streams of visual letters. Colored letters embedded within the streams indicated which stream was to be used for target detection, signaling that participants should “hold” or “shift” their current focus of spatial attention. A behavioral experiment comparing performance in these focused-attention conditions with performance in a divided-attention condition confirmed the efficacy of the spatial cues. Another behavioral experiment showed that overt shifts of spatial attention were mainly complete by around 400 msec, placing an upper boundary for isolating neural activity that was instrumental in controlling spatial shifts. Event-related potentials recorded during a covert version of the focused-attention task showed a large amount of nonlateralized neural activity associated with spatial shifts, with significant effects starting around 330 msec. The effects started over posterior scalp regions, where they remained pronounced. Transient effects were also observed over frontal scalp regions. The results are compatible with a pivotal role of posterior parietal areas in initiating shifts of spatial attention.