Chlorpyrifos (CPF) is an organophosphorus (OP) insecticide used extensively in agricultural and residential settings. Gestational, sub-acute exposure to CPF is linked to an increased incidence of neurodevelopmental disorders in children. Animal studies have modeled these neurobehavioral detriments and identified lasting increases in serotonergic (5-HT) receptor expression. However, the functional alterations in the brain induced by this exposure remain largely unknown. To address this, we used a rat model of gestational CPF exposure to interrogate the alterations in the developing somatosensory (barrel) cortex. Rat dams were exposed to CPF (5 mg/kg) or vehicle on gestational days 18-21 via subcutaneous injection with no overt acute toxicity. We performed whole-cell patch clamp recordings of pyramidal neurons in the barrel cortex on postnatal days 12 through 20 in both male and female progeny. A spike timing dependent plasticity protocol revealed a disruption to the normal development of long-term synaptic depression in CPF-exposed offspring. The frequency of spontaneous inhibitory postsynaptic currents and paired-pulse ratios were higher, and the frequency of miniature inhibitory postsynaptic currents were lower in pyramidal neurons from CPF-exposed offspring. These findings suggest a presynaptic mechanism of inhibited GABA release, with potential disinhibition of inhibitory neurons. Histological evaluation of barrel cortex indicated that gestational exposure to CPF disrupted normal barrel field patterning, increasing the septal area and total barrel field area. A cell-attached patch clamp method additionally revealed a marked increase in the number of spontaneously firing neurons. Immunohistochemical labeling of c-Fos, a marker of neuronal activity, revealed a pronounced increase in c-Fos expression in neurons of juvenile and adult rats that had been gestationally exposed to CPF. RNAscope in situ hybridization showed an increase in the expression of the receptor 5-HT1B in PV neurons in the barrel cortex of CPF-exposed rats. These data demonstrate that gestational exposure to the OP insecticide CPF disrupts plasticity, GABAergic synaptic transmission and the structural integrity in the rat barrel cortex during brain development. These neurophysiological effects may contribute to the established behavioral outcomes resulting from gestational exposures to CPF and offer guidance for novel preventative interventions.