Significance Our work tackles a current debate regarding working memory (WM). Traditionally, this ability to maintain and manipulate information has been thought to require conscious processing and persistent neural activity. Recent evidence challenges this assumption: Information may be briefly stored without conscious awareness and sustained neural activity. Here, we reconcile these competing views. We recorded brain activity while adults remembered or mentally rotated subjectively visible or invisible stimuli. We showed that the mere short-term storage of information may proceed without consciousness or persistent neural activity. However, manipulating information in WM during rotation required both. Thus, non-conscious, activity-silent maintenance is a genuine phenomenon but should be termed “activity-silent short-term memory”; when using a memory, a reactivation, associated with conscious reportability, is necessary. , Two types of working memory (WM) have recently been proposed: ( i ) active WM, relying on sustained neural firing, and ( ii ) activity-silent WM, for which firing returns to baseline, yet memories may be retained by short-term synaptic changes. Activity-silent WM in particular might also underlie the recently discovered phenomenon of non-conscious WM, which permits even subliminal stimuli to be stored for several seconds. However, whether both states support identical forms of information processing is unknown. Theory predicts that activity-silent states are confined to passive storage and cannot operate on stored information. To determine whether an explicit reactivation is required before the manipulation of information in WM, we evaluated whether participants could mentally rotate brief visual stimuli of variable subjective visibility. Behaviorally, even for unseen targets, subjects reported the rotated location above chance after several seconds. As predicted, however, at the time of mental rotation, such blindsight performance was accompanied by ( i ) neural signatures of consciousness in the form of a sustained desynchronization in alpha/beta frequency and ( ii ) a reactivation of the memorized information as indicated by decodable representations of participants’ guess and response. Our findings challenge the concept of genuine non-conscious “working” memory, argue that activity-silent states merely support passive short-term memory, and provide a cautionary note for purely behavioral studies of non-conscious information processing.