Visual attention can be focused concurrently on two stimuli at noncontiguous locations while intermediate stimuli remain ignored. Nevertheless, behavioral performance in multifocal attention tasks falters when attended stimuli fall within one visual hemifield as opposed to when they are distributed across left and right hemifields. This “different-hemifield advantage” has been ascribed to largely independent processing capacities of each cerebral hemisphere in early visual cortices. Here, we investigated how this advantage influences the sustained division of spatial attention. We presented six isoeccentric light-emitting diodes (LEDs) in the lower visual field, each flickering at a different frequency. Participants attended to two LEDs that were spatially separated by an intermediate LED and responded to synchronous events at to-be-attended LEDs. Task-relevant pairs of LEDs were either located in the same hemifield (“within-hemifield” conditions) or separated by the vertical meridian (“across-hemifield” conditions). Flicker-driven brain oscillations, steady-state visual evoked potentials (SSVEPs), indexed the allocation of attention to individual LEDs. Both behavioral performance and SSVEPs indicated enhanced processing of attended LED pairs during “across-hemifield” relative to “within-hemifield” conditions. Moreover, SSVEPs demonstrated effective filtering of intermediate stimuli in “across-hemifield” condition only. Thus, despite identical physical distances between LEDs of attended pairs, the spatial profiles of gain effects differed profoundly between “across-hemifield” and “within-hemifield” conditions. These findings corroborate that early cortical visual processing stages rely on hemisphere-specific processing capacities and highlight their limiting role in the concurrent allocation of visual attention to multiple locations.