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Introduction Poor prenatal sleep health is a pervasive reproductive health concern that informs the health of the mother and fetal development. Despite the almost ubiquitous nature of sleep disturbances across pregnancy, sleep health within pregnant populations, and its effects on the next generation, remain poorly studied. We recently showed that prenatal maternal sleep quality predicts newborn hippocampal volume. However, the relation between prenatal sleep quality and neonatal neural circuit development remains unknown. Changes in neonatal white matter microstructure presage compromised socioemotional and cognitive health, including the development of psychopathology and neurocognitive disorders, making it a plausible neurobiological pathway linking prenatal maternal sleep and offspring socioemotional health. This study first examined the relations between trajectories of prenatal maternal sleep quality and subsequent neonatal white matter integrity. We next evaluated whether neonatal white matter integrity partially mediates associations between prenatal sleep and infant negative emotionality. Methods Pregnant participants (n = 116) provided prospective and longitudinal data of prenatal maternal sleep quality at 16, 29, and 35 gestational weeks using the Pittsburgh Sleep Quality Index. Neonatal (53% female) white matter integrity was assessed via diffusion weighed images using magnetic resonance imaging (MRI). Infant negative emotionality was collected at 6 postpartum months using the Infant Behavior Questionnaire. Results Trajectories of prenatal maternal sleep quality predicted higher bilateral neonatal fractional anisotropy (FA) in the uncinate fasciculus (e.g., right: b = 0.15, p = .023). Further, higher uncinate FA predicted more infant negative emotionality (e.g., right: b = 0.25, p = .011) and uncinate FA partially mediated the association between prenatal maternal sleep and infant negative emotionality (right: indirect effect = 0.014, CI = [.0001, .0323], p < .05). Associations remained after covarying for infant postconceptional age at MRI, motion in MRI scan, sex, and income-to-needs ratio. Conclusion These findings highlight prenatal maternal sleep health as a prenatal signal with intergenerational connections to offspring neurobiology and negative emotionality, both of which have been previously implicated in the development of psychopathology. Pregnancy is a sensitive period in which interventions may inform the health of two generations. Support (if any) NIMH R01MH109662, NHLBI R01HL155744, and diversity training supplement for 1st author; F32MH125572 for 2nd author.