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Recent studies suggest that parental caregiving is associated with adaptive changes in neurocognitive responses to emotional cues and oxytocin function, possibly reflecting the increased need of parents to monitor infants’ emotional states. In the current study, we investigated whether the changes associated with motherhood and oxytocin receptor genetic variation rs53576 are specific to the processing of infant cues as opposed to a more general increase in responsiveness to emotional cues. We measured event-related brain potentials (ERPs) and behavioral recognition responses from mothers of young infants (n = 48) and nulliparous females (n = 46) to infant and adult faces displaying strong and mild intensity emotional expressions. Mothers and GG allele carriers of the OXTR gene showed an early latency (∼100 ms) differential frontal ERP response to strong intensity facial expressions, and mothers also showed modulation of the posterior EPN waveform by negative valence. The early frontal ERP modulation was associated with faster emotion recognition performance across participants. Most importantly, these effects were highly specific to infant facial expressions. The results point to a dissociable neurocognitive system that is involved in monitoring infants’ emotional cues and may be important in supporting parental caregiving in humans.