•  Zinc inhibits ionotropic receptors commonly found at central synapses, as well as a wide variety of voltage‐activated ion channels that modulate neuronal excitability and neurotransmitter release. •  We found that zinc chelation facilitated GABAergic signalling in dentate granule cells and that blocking T‐type Ca2+ channel activity abolished this effect. Zinc chelation reduced spike threshold, increased spike width and shifted the input–output relationship in dentate interneurones, which is consistent with increased excitability. •  In granule cells, zinc chelation narrowed the window for the integration of glutamatergic inputs originating from perforant path synapses. •  These results demonstrate that zinc modulates dentate interneurone function and regulates spike routing to local and hippocampal targets. Abstract  Zinc actions on synaptic transmission span the modulation of neurotransmitter receptors, transporters, activation of intracellular cascades and alterations in gene expression. Whether and how zinc affects inhibitory synaptic signalling in the dentate gyrus remains largely unexplored. We found that mono‐ and di‐synaptic GABAergic inputs onto dentate granule cells were reversibly depressed by exogenous zinc application and enhanced by zinc chelation. Blocking T‐type Ca2+ channels prevented the effect of zinc chelation. When recording from dentate fast‐spiking interneurones, zinc chelation facilitated T‐type Ca2+ currents, increased action potential half‐width and decreased spike threshold. It also increased the offset of the input–output relation in a manner consistent with enhanced excitability. In granule cells, chelation of zinc reduced the time window for the integration of glutamatergic inputs originating from perforant path synapses, resulting in reduced spike transfer. Thus, zinc‐mediated modulation of dentate interneurone excitability and GABA release regulates information flow to local targets and hippocampal networks.