The basolateral nucleus of the amygdala (BLA) receives cholinergic innervation from the basal forebrain and nicotine, via activation of neuronal nicotinic acetylcholine receptors (nAChRs), can improve performance in amygdala-based learning tasks. We tested the hypothesis that acute and prenatal nicotine exposure modulates cortico-amygdala synaptic transmission. We found, that low dose, single trial exposures to nicotine can elicit lasting facilitation, the extent of which is dependent on the level of stimulation of the cortical inputs to the BLA. In addition, sustained facilitation is ablated by prenatal exposure to nicotine. This study examined synaptic transmission in 238 patch clamp recordings from BLA neurons in acute slice from mouse brain. Pharmacological studies in wild type and nAChR subunit knock-out mice reveal that activation of presynaptic 7 containing (7*) and non 7 nAChRs facilitates glutamatergic transmission in an activity-dependent manner. Without prior stimulation, application of nicotine elicits modest and transient facilitation of glutamatergic postsynaptic currents (PSCs) in ~40% BLA neurons. With low frequency stimulation of cortical inputs nicotine elicits robust facilitation of transmission at ~60% of cortico-BLA synapses and synaptic strength remains elevated at ~40% of these connections for more than 15 minutes after nicotine washout. Following paired pulse stimulation nicotine elicits long-lasting facilitation of glutamatergic transmission at ~70% of cortico-BLA connections. Nicotine reduces the threshold for activation of LTP of cortico-BLA synapses evoked by patterned stimulation. Prenatal exposure to nicotine reduced subsequent modulatory responses to acute nicotine application.