The prefrontal hemispheres must coordinate dynamically to maintain a unified representation of visual space. Recently, two opposing theories using distinct storage strategies have been proposed: A high-capacity specialized architecture, where each hemisphere governs contralateral behavior, and a fail-safe redundant one, where both hemispheres jointly guide behavior across the visual space. To determine the neural architecture underlying interhemispheric coordination, we analyzed simultaneous bilateral prefrontal cortex recordings from three macaque monkeys performing a visuo-spatial working memory task. Both hemispheres equally predicted behavioral imprecisions across the visual field and decoding errors were weakly correlated between hemispheres, suggesting a redundant, weakly coupled organization. Attractor network simulations showed that redundancy improved precision when task demands were below memory capacity, while weak interhemispheric coupling increased capacity in more demanding tasks by allowing hemispheric specialization. This interhemispheric architecture reconciles previous findings thought to support distinct models into a unified architecture, revealing a versatile interhemispheric architecture that adapts to varying cognitive demands.