Behavioral evidence suggests that the use of implicitly learned spatial contexts for improved visual search may depend on visual working memory resources. Working memory may be involved in contextual cueing in different ways: (1) For keeping implicitly learned working memory contents available during search or (2) for the capture of attention by contexts retrieved from memory. We mapped brain areas that were modulated by working memory capacity. Within these areas, activation was modulated by contextual cueing along the descending segment of the intraparietal sulcus, an area that has previously been related to maintenance of explicit memories. Increased activation for learned displays, but not modulated by the size of contextual cueing, was observed in temporo-parietal junction area, previously associated with capture of attention by explicitly retrieved memory items, and in ventral visual cortex. This pattern of activation extends previous research on dorsal versus ventral stream functions in memory guidance of attention to the realm of attentional guidance by implicit memory.