Individuals with borderline personality disorder (BPD) commonly display deficits in emotion regulation, but findings in the area of social cognitive (e.g., theory of mind, ToM) capacities have been heterogeneous. The aims of the current study were to investigate differences between patients with BPD and controls in functional connectivity (1) between the emotion and ToM network and (2) in the default mode network (DMN). Functional magnetic resonance imaging was used to investigate 19 healthy controls and 17 patients with BPD at rest and during ToM processing. Functional coupling was analysed. Significantly decreased functional connectivity was found for patients compared with controls between anterior cingulate cortex and three brain areas involved in ToM processes: the left superior temporal lobe, right supramarginal/inferior parietal lobes, and right middle cingulate cortex. Increased functional connectivity was found in patients compared with controls between the precuneus as the DMN seed and the left inferior frontal lobe, left precentral/middle frontal, and left middle occipital/superior parietal lobes during rest. Reduced functional coupling between the emotional and the ToM network during ToM processing is in line with emotion-regulation dysfunctions in BPD. The increased connectivity between precuneus and frontal regions during rest might be related to extensive processing of internal thoughts and self-referential information in BPD.