The posterior cingulate cortex (pCC) often deactivates during complex tasks, and at rest is often only weakly correlated with regions that play a general role in the control of cognition. These observations led to the hypothesis that pCC contributes to automatic aspects of memory retrieval and cognition. Recent work, however, has suggested that the pCC may support both automatic and controlled forms of memory processing and may do so by changing its communication with regions that are important in the control of cognition across multiple domains. The current study examined these alternative views by characterising the functional coupling of the pCC in easy semantic decisions (based on strong global associations) and in harder semantic tasks (matching words on the basis of specific non-dominant features). Increasingly difficult semantic decisions led to the expected pattern of deactivation in the pCC; however, psychophysiological interaction analysis revealed that, under these conditions, the pCC exhibited greater connectivity with dorsolateral prefrontal cortex (PFC), relative to both easier semantic decisions and to a period of rest. In a second experiment using different participants, we found that functional coupling at rest between the pCC and the same region of dorsolateral PFC was stronger for participants who were more efficient at semantic tasks when assessed in a subsequent laboratory session. Thus, although overall levels of activity in the pCC are reduced during external tasks, this region may show greater coupling with executive control regions when information is retrieved from memory in a goal-directed manner.