Excessive alcohol consumption during adolescence is regarded as a risk factor for the development of alcoholism later in life, but the pathophysiological mechanisms that render the adult brain susceptible to alcohol are largely unknown. GABAA receptors are among the targets of alcohol to regulate neural activity in the brain. Work from our lab has demonstrated that activin, a member of the TGF-β family, controls alcohol potentiation of GABAA receptors in adult mouse dorsal hippocampus. Considering the well-known functional segregation along the hippocampal longitudinal axis, we examined here how adolescent alcohol drinking affects GABAergic inhibition and its response upon alcohol re-exposure in adulthood, using whole-cell voltage-clamp recordings from dentate gyrus granule cells in dorsal and ventral hippocampal slices from adult mice (3-4 months old). Compared to wild-type control mice, heavy drinking in the dark (20% alcohol, two-bottle choice paradigm) between postnatal days 30 and 45 produced a long-lasting reduction in synaptic and extra-synaptic GABAergic inhibition in ventral, but not dorsal granule cells. Inhibitory synaptic drive onto adult granule cells of either region from adolescent drinking mice showed less enhancement upon acute alcohol exposure than those from alcohol-naïve mice. Interestingly, we hardly observed such lasting effects of adolescent drinking in transgenic mice expressing a dominant-negative mutant of activin receptors IB (dnActRIB). Our results reveal a number of sustained and partially hippocampal region-specific effects of heavy adolescent drinking, and suggest a role of activin signaling in controlling the impact of alcohol consumption on inhibitory neurotransmission at different stages of life.