Primate brain development is shaped by inputs received during critical periods. These inputs differ between independent and cooperative breeders: in cooperative breeders infants interact with multiple caregivers. We study how the neurodevelopmental timing of the cooperatively breeding common marmoset maps onto behavioral milestones. To obtain structure-function co-constructions we combine behavioral, neuroimaging (anatomical and functional) and neural tracing experiments. We find that brain areas critically involved in observing conspecifics interacting: (i) develop in clusters; (ii) have prolonged developmental trajectories; (iii) differentiate during the period of negotiations between immatures and multiple caregivers; (iv) do not share stronger connectivity than with other regions. The developmental timing of social brain areas correlates with social and behavioral milestones in marmosets and, as in humans, extends into adulthood. This rich social input is likely critical for the emergence of their strong socio-cognitive skills. Since humans are cooperative breeders too, these findings have strong implications for the evolution of human social cognition.