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Visually guided behavior relies on the integration of sensory input and information held in working memory (WM). Yet it remains unclear how this is accomplished at the level of neural circuits. We studied the direct visual cortical inputs to neurons within a visuomotor area of prefrontal cortex in behaving monkeys. We show that the efficacy of visual input to prefrontal cortex is gated by information held in WM. Surprisingly, visual input to prefrontal neurons was found to target those with both visual and motor properties, rather than preferentially targeting other visual neurons. Furthermore, activity evoked from visual cortex was larger in magnitude, more synchronous, and more rapid, when monkeys remembered locations that matched the location of visual input. These results indicate that WM directly influences the circuitry that transforms visual input into visually guided behavior.