Sleep promotes memory consolidation, a process by which fresh and labile memories are reorganized into stable memories. Emotional memories are usually better remembered than neutral ones, even at long retention delays. In this study, we assessed the influence of sleep during the night after encoding onto the neural correlates of recollection of emotional memories 6 months later. After incidental encoding of emotional and neutral pictures, one-half of the subjects were allowed to sleep, whereas the others were totally sleep deprived, on the first postencoding night. During subsequent retest, functional magnetic resonance imaging sessions taking place 3 d and 6 months later, subjects made recognition memory judgments about the previously studied and new pictures. Between these retest sessions, all participants slept as usual at home. At 6 month retest, recollection was associated with significantly larger responses in subjects allowed to sleep than in sleep-deprived subjects, in the ventral medial prefrontal cortex (vMPFC) and the precuneus, two areas involved in memory retrieval, as well as in the extended amygdala and the occipital cortex, two regions the response of which was modulated by emotion at encoding. Moreover, the functional connectivity was enhanced between the vMPFC and the precuneus, as well as between the extended amygdala, the vMPFC, and the occipital cortex in the sleep group relative to the sleep-deprived group. These results suggest that sleep during the first postencoding night profoundly influences the long-term systems-level consolidation of emotional memory and modifies the functional segregation and integration associated with recollection in the long term.