Mentalizing is defined as the ability to attribute mental states to oneself and others. In the context of parental behavior, parents' tendency to comment on their child's mental activities refers to the concept of mind-mindedness (MM). MM has been positively associated with various developmental outcomes in children, notably their own ability to mentalize, known as theory of mind (ToM). Although parental (MM) and child (ToM) mentalizing have important implications during childhood, their associations with children's neural structures are largely unknown. Among 62 mother-child dyads, maternal MM was rated from free-play sequences when children were aged 1 year, child ToM was assessed using a first-order false-belief task at 4 years of age, and structural MRI images were acquired at 10 years of age. Maternal MM was positively associated with gray matter volumes (GMV) in the dorsal prefrontal cortex and the superior temporal pole. Child ToM abilities were positively associated with GMV in the ventromedial prefrontal cortex. Though cortical regions associated with MM and ToM showed no anatomical overlap, many are functionally connected through a neural network highly involved in self-referential strategies for mentalizing. These findings suggest that MM and ToM may contribute to distinct sub-processes that collectively support social cognition development.