Key points Acute pancreatitis is one of the most severe disorders of the exocrine pancreas. Pancreatic exocrine secretions (PES) are under regulatory control of dorsal motor nucleus of the vagus (DMV) neurones and their activity is regulated by inhibitory GABAergic and excitatory glutamatergic synaptic inputs. Group II metabotropic glutamate receptors (mGluR) decrease synaptic transmission to pancreas‐projecting DMV neurones and modulate PES. In this study, we show that acute pancreatitis induces a long‐lasting increase in excitatory synaptic transmission to pancreas‐projecting neurones by decreasing the response of excitatory synaptic terminals to group II mGluR agonists. These data suggest that changes in group II mGluR expression in the DMV may underlie short‐ and long‐term changes in PES in acute pancreatitis. Abstract Recent studies have shown that pancreatic exocrine secretions (PES) are modulated by dorsal motor nucleus of the vagus (DMV) neurones, whose activity is finely tuned by GABAergic and glutamatergic synaptic inputs. Group II metabotropic glutamate receptors (mGluR) decrease synaptic transmission to pancreas‐projecting DMV neurones and increase PES. In the present study, we used a combination of in vivo and in vitro approaches aimed at characterising the effects of caerulein‐induced acute pancreatitis (AP) on the vagal neurocircuitry modulating pancreatic functions. In control rats, microinjection of bicuculline into the DMV increased PES, whereas microinjections of kynurenic acid had no effect. Conversely, in AP rats, microinjection of bicuculline had no effect, whereas kynurenic acid decreased PES. DMV microinjections of the group II mGluR agonist APDC and whole cell recordings of excitatory currents in identified pancreas‐projecting DMV neurones showed a reduced functional response in AP rats compared to controls. Moreover, these changes persisted up to 3 weeks following the induction of AP. These data demonstrate that AP increases the excitatory input to pancreas‐projecting DMV neurones by decreasing the response of excitatory synaptic terminals to group II mGluR agonist.