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Multiple types of memory guide attention: Both long-term memory (LTM) and working memory (WM) effectively guide visual search. Furthermore, both types of memories can capture attention automatically, even when detrimental to performance. It is less clear, however, how LTM and WM cooperate or compete to guide attention in the same task. In a series of behavioral experiments, we show that LTM and WM reliably cooperate to guide attention: Visual search is faster when both memories cue attention to the same spatial location (relative to when only one memory can guide attention). LTM and WM competed to guide attention in more limited circumstances: Competition only occurred when these memories were in different dimensions – particularly when participants searched for a shape and held an accessory color in mind. Finally, we found no evidence for asymmetry in either cooperation or competition: There was no evidence that WM helped (or hindered) LTM-guided search more than the other way around. This lack of asymmetry was found despite differences in LTM-guided and WM-guided search overall, and differences in how two LTMs and two WMs compete or cooperate with each other to guide attention. This work suggests that, even if only one memory is currently task-relevant, WM and LTM can cooperate to guide attention; they can also compete when distracting features are salient enough. This work elucidates interactions between WM and LTM during attentional guidance, adding to the literature on costs and benefits to attention from multiple active memories.