Successful recovery after nervous system injury requires not only the restoration of damaged projections, but also appropriate processing of restored input by downstream circuits. How do target circuits adapt to such conditions of denervation and re-innervation? Might they undergo adaptive plastic modifications that promote functional repair and recovery? We addressed these questions by studying a unique model of naturally occurring regeneration in the adult mammalian brain. After a single dose of the olfactotoxin methimazole, olfactory sensory neurons in the nasal olfactory epithelium degenerate and are subsequently replaced via local neurogenesis. This process leaves their target structure in the brain – the olfactory bulb (OB) – transiently denervated before being reinnervated by new axonal inputs. Using ex vivo acute slice electrophysiology and immunohistochemistry, we studied the changes occurring in OB circuits during this process of naturally occurring input regeneration. We found that during the initial phases of re-innervation the input-output gain of the OB was strikingly elevated, with stronger projection neuron spiking in response to a given strength of axonal input stimulation. Input strength itself was weaker during this period, and we saw no changes in projection neuron excitability nor deep-layer OB inhibition. In contrast, we found evidence for elevated local excitation and decreased local inhibition in superficial glomerular networks, suggesting that alterations in input-level circuitry underlie regeneration-associated changes in input-output gain. Via such plastic mechanisms, target circuits may maximise the impact of information that is just beginning to return from regenerating inputs, thus facilitating functional recovery from injury.