Maternal motivation enables heightened responsivity of mothers towards offspring. While this motivational state is critical to infant survival, little is known about its regulation. Previous work in maternal rodents demonstrates that lesioning ventral tegmental area (VTA) neurons disrupts maternal motivated behaviors; and that these behaviors are restored by manipulating pup sensory salience (i.e., by increasing pup cries) and maternal states (Hansen 1994 Physiol Behav). Additionally, the neurohormone oxytocin is known to promote VTA-mediated maternal behaviors including infant approach and nursing (Pedersen et al., 1994 Behav Neurosci). What remains unclear is how information about infant needs and internal states of the mother are integrated in the VTA to determine the overall levels of maternal motivation that drive context-specific offspring care. Here, we show that infant cues are signaled to the VTA by oxytocin and that this sensory input, along with internal state, modulates maternal motivation. We used a combination of anatomical tracings and recordings in brain slices to identify a noncanonical auditory pathway relaying acoustic information about infant cries via the posterior intralaminar thalamus (PIL) to hypothalamic oxytocin neurons. We performed fiber photometry from oxytocin neurons in awake maternal mice (dams), and found that these cells are activated by pup distress vocalizations. The thalamus-hypothalamus auditory pathway gates oxytocin release in the VTA and maternal behavior in response to calls. We further show that internal states regulate maternal motivation by exploring the effect on pup-oriented behaviors of dams which were temporarily separated from their litters. Our results provide a mechanism for the transformation of sensory cues from the offspring into hormonal output in maternal motivational networks which, together with the contribution of internal states, sustain maternal arousal and pup-oriented behaviors.