Despite the limited knowledge on the safety of Cannabidiol (CBD) during pregnancy, pregnant women often use CBD to alleviate various pregnancy-related symptoms such as nausea, insomnia, anxiety, and chronic pain. While CBD can cross the human placenta, potentially affecting fetal development, the long-term consequences of prenatal CBD exposure remain poorly understood. The insular cortex (IC), a crucial brain region involved in multisensory and emotional processing, consists of two distinct subregions: the anterior IC (aIC), responsible for processing emotional and social signals, and the posterior IC (pIC), specialized in interoception and pain perception. Due to its extensive connections with other brain areas, the IC has been implicated in the development of psychiatric disorders. Previously, our research demonstrated that under normal physiological conditions, the aIC and pIC neurons have distinct properties. In this study, we conducted electrophysiological characterizations of IC principal neurons to investigate how exposure to low doses of CBD during gestation (3 mg/kg subcutaneously) affects the cellular properties of aIC and pIC neurons in male and female offspring. Our findings indicate that prenatal CBD leads to multiple alterations in the active and passive membrane properties, as well as the intrinsic excitability of IC neurons. These effects are observed in a sex- and subregion-specific manner. Strikingly, the normal aIC/pIC dichotomy disappears after prenatal CBD, resulting in the loss of differentiation between IC subregions in both sexes. Together, these results suggest a sexual divergence in the effects of prenatal CBD, which may have implications for the development of adult psychopathology.