Theory of Mind, empathy, and action observation are central themes in social neuroscience research. Meta-analyses of functional neuroimaging studies show substantial heterogeneity in brain activation for these cognitive abilities, depending on the type of experimental task used. We followed up on these findings by a comparison to basic connectivity networks of the brain. In particular, we evaluated to what extent brain activation for social cognition tasks draws on areas of different fMRI resting-state networks (e.g., Default Mode, Ventral Attention Network) in parallel. Our review illustrates high prevalence of such network co-recruitments across Theory of Mind, empathy, and action observation tasks. To characterize these observations in more detail, we additionally conducted a literature review of fMRI effective connectivity studies. Findings reveal two main types of cross-network interactions in social cognition tasks: Negative coupling (segregation) between Default Mode and Control Networks (Ventral Attention, Frontoparietal, and Dorsal Attention Network), and positive coupling (integration) between these networks. The two patterns reflect different types of brain network organization taking place in the context of social cognition tasks–segregation for specialized, versus integration for flexible processing. We discuss evidence from connectivity research in other research fields, suggesting that increased network integration indicates more effortful and controlled processing. Based on that, we consider how findings of network segregation versus integration can provide new perspectives on dual-system accounts of social cognition, which differentiate between automatic and controlled processes. Moreover, we discuss how the reviewed evidence relates to neural processes which are assumed to take place during naturalistic social cognition.