Vocal production learning (the capacity to learn to produce vocalizations) is a multidimensional trait that involves different learning mechanisms during different temporal and socioecological contexts. Key outstanding questions are whether vocal production learning begins during the embryonic stage and whether mothers play an active role in this through pupil-directed vocalization behaviors. We examined variation in vocal copy similarity (an indicator of learning) in eight species from the songbird family Maluridae, using comparative and experimental approaches. We found that (1) incubating females from all species vocalized inside the nest and produced call types including a signature “B element” that was structurally similar to their nestlings’ begging call; (2) in a prenatal playback experiment using superb fairy wrens (Malurus cyaneus), embryos showed a stronger heart rate response to playbacks of the B element than to another call element (A); and (3) mothers that produced slower calls had offspring with greater similarity between their begging call and the mother’s B element vocalization. We conclude that malurid mothers display behaviors concordant with pupil-directed vocalizations and may actively influence their offspring’s early life through sound learning shaped by maternal call tempo.