After information is encoded into memory, it undergoes an off-line period of consolidation that may occur optimally during sleep. The consolidation process not only solidifies memories but also changes them in useful and adaptive ways. Here, we provide evidence for a shift in the neural structures used to retrieve emotional memories after a night of sleep compared to a day of wakefulness. Although the hippocampus was activated during successful retrieval of negative objects regardless of whether participants slept during a delay, sleep led to a shift from engagement of a diffuse memory retrieval network—including widespread activity in the lateral prefrontal and parietal cortices—to a more refined network of regions—including the amygdala and ventromedial pFC. Effective connectivity analyses revealed stronger connections among limbic regions after sleep versus wake. Although circadian effects may have contributed to these findings, our data strongly suggest that a night of sleep is sufficient to evoke qualitative changes in the emotional memory retrieval network.