How closely related are the social and communicative impairments in Autism Spectrum Disorder (ASD)? Recent findings in typically developing children suggest that both types of impairment are highly heritable but have only moderate behavioural and genetic overlap. So far, their respective roles in social perception are poorly understood. Here we show that when looking at other people’s faces, children with ASD who are better at socio-emotional behaviours than non-verbal communication look more at the eyes, while those with the opposite profile look more at the mouth (Study 1). For the mouth area, a similar pattern was observed for inverted faces, suggesting that information from this area is perceived on a featural basis. In Study 2, we found that when shown a person performing manual actions, ‘eye-lookers’ from Study 1 tended to look most at the face of the actor, while ‘mouth-lookers’ from Study 1 tended to look at the action itself (hand/objects). This result was found in both ASD and typical development. In Study 3, the main finding in Study 1 was replicated in a new sample. Taken together, we interpret these results as supporting the view that the neural systems underlying socio-emotional versus non-verbal communication skills are separable, a finding that has important theoretical and clinical implications. The results also suggest that a similar differentiation of looking behaviour may operate in normal development.