Postnatal depression (PND) increases the risk of neurodevelopmental impairments in offspring, yet the underlying mechanisms remain elusive. Here, we identify an intergenerational signaling pathway through which maternal psychological state is encoded in breastmilk microRNAs (miRNAs) and transmitted to offspring via breastmilk small extracellular vesicles (sEVs). Using cross-fostering models, we demonstrate that maternal depression disrupts the maturation of newborn neurons in the offspring hippocampal dentate gyrus (DG), leading to cognitive deficits and depressive-like behaviors. Strikingly, gastric administration of PND-derived breastmilk sEVs to healthy pups recapitulates these neurodevelopmental phenotypes. Mechanistically, PND-induced miRNAs are packaged into breastmilk sEVs and delivered to infant brain, where they suppress mGluR8 expression in supramammillary nucleus (SuM) neurons projecting to the DG. This presynaptic mGluR8 deficiency dysregulates glutamate release, triggers aberrant synaptic transmission and calcium overload, and ultimately drives a pathological “high-frequency, low amplitude” neuronal activation pattern that compromises the functional integration of newborn neurons into hippocampal circuits. Critically, inhibiting sEV secretion from the mammary gland or sequestering the culprit miRNAs within offspring SuM neurons rescues these neurodevelopmental deficits. Together, these findings establish breastmilk sEV miRNAs as an epigenetic vector that translates maternal psychological state into maladaptive programming of offspring brain circuitry and behavior.