IgG autoantibodies against the GluN1 (NR1) subunit of NMDA receptors underlie the most common form of autoimmune encephalitis, but they are also found in asymptomatic individuals with a reported seroprevalence of up to 1%. Maternal NR1 autoantibodies may actively cross the placenta during pregnancy, reaching the developing brain through the immature blood-brain barrier. However, to what extent prenatal exposure to NR1 autoantibodies influences neuronal circuit maturation remains elusive. We address this question in hippocampal area CA1 using a murine passive-transfer model, in which human monoclonal NR1 or non-reactive isotype-matched control autoantibodies are intraperitoneally administered to pregnant dams. At birth, NR1 autoantibodies are found in a puncta-like pattern mainly in distal dendritic layers. Electrophysiological recordings reveal a selective impairment of GABAergic transmission in CA1 pyramidal cells, while glutamatergic signaling remains unaffected. At the circuit level, placentally transferred NR1 autoantibodies profoundly attenuate spontaneous synchronized activity in CA1. We reconcile these experimental findings using a dynamic systems modeling approach. Collectively, our study demonstrates that placentally transferred NR1 autoantibodies impair hippocampal circuit development in vivo, pointing to a novel and potentially important mechanism of neurodevelopmental disease.