Plants have evolved complex mechanisms that allow them to withstand multiple environmental stresses, including biotic and abiotic stresses. Here, we investigated the interaction between herbivore exposure and salt stress of Ammopiptanthus nanus, a desert shrub. We found that jasmonic acid (JA) was involved in plant responses to both herbivore attack and salt stress, leading to an increased NaCl stress tolerance for herbivore‐pretreated plants and increase in K+/Na+ ratio in roots. Further evidence revealed the mechanism by which herbivore improved plant NaCl tolerance. Herbivore pretreatment reduced K+ efflux and increased Na+ efflux in plants subjected to long‐term, short‐term, or transient NaCl stress. Moreover, herbivore pretreatment promoted H+ efflux by increasing plasma membrane H+‐adenosine triphosphate (ATP)ase activity. This H+ efflux creates a transmembrane proton motive force that drives the Na+/H+ antiporter to expel excess Na+ into the external medium. In addition, high cytosolic Ca2+ was observed in the roots of herbivore‐treated plants exposed to NaCl, and this effect may be regulated by H+‐ATPase. Taken together, herbivore exposure enhances A. nanus tolerance to salt stress by activating the JA‐signalling pathway, increasing plasma membrane H+‐ATPase activity, promoting cytosolic Ca2+ accumulation, and then restricting K+ leakage and reducing Na+ accumulation in the cytosol.