While empathy and Theory of Mind (ToM) have classically been studied as separate social functions, recent advances demonstrate the need to investigate the two in interaction: Naturalistic settings often blur the distinction of affect and cognition and demand the simultaneous processing of such different stimulus dimensions. Here, we investigate how empathy and ToM related brain networks interact in contexts wherein multiple cognitive and affective demands must be processed simultaneously. Building on the findings of a recent meta-analysis and hierarchical clustering analysis, we perform meta-analytic connectivity modeling to determine patterns of task-context specific network changes. We analyze 140 studies including classical empathy and ToM tasks, as well as complex social tasks. For studies at the intersection of empathy and ToM, neural co-activation patterns included areas typically associated with both empathy and ToM. Network integration is discussed as a means of combining mechanisms across unique behavioral domains. Such integration may enable adaptive behavior in complex, naturalistic social settings that require simultaneous processing of a multitude of different affective and cognitive information.