Spatial attention can be oriented endogenously, based on current task goals, or exogenously, triggered by salient events in the environment. Based upon literature demonstrating differences in the time course and neural substrates of each type of orienting, these two attention systems are often treated as fundamentally distinct. However, recent studies suggest that rhythmic neural activity in the alpha band (8–13 Hz) and slow waves in the event-related potential (ERP) may emerge over parietal-occipital cortex following both endogenous and exogenous attention cues. To assess whether these neural changes index common processes of spatial attention, we conducted two within-subject experiments varying the two main dimensions over which endogenous and exogenous attention tasks typically differ: cue informativity (spatially predictive vs. non-predictive) and cue format (centrally vs. peripherally presented). This task design allowed us to tease apart neural changes related to top-down goals and those driven by the reflexive orienting of spatial attention, and examine their interactions in a novel hybrid cross-modal attention task. Our data demonstrate that both central and peripheral cues elicit lateralized ERPs over parietal-occipital cortex, though at different points in time, consistent with these ERPs reflecting the orienting of spatial attention. Lateralized alpha activity was also present across all tasks, emerging rapidly for peripheral cues and sustaining longer for spatially informative cues. Overall, these data indicate that distinct slow-wave ERPs index the spatial orienting of endogenous and exogenous attention, while lateralized alpha activity represents a common signature of visual-cortical biasing in anticipation of potential targets across both types of attention.