(Z)–3–hexenol, a small gaseous molecule, is produced in plants under biotic stress and induces defense responses in neighboring plants. However, the research on little is known about how (Z)–3–hexenol induces plant defense–related signaling. In this study, we uncovered how (Z)–3–hexenol treatment enhances insect resistance by increasing γ–aminobutyric acid (GABA) contents in Arabidopsis thaliana leaves. First, (Z)–3–hexenol increases the intracellular content of the signaling molecule calcium in Arabidopsis leaf mesophyll cells. Both intracellular and extracellular calcium stores regulate these changes in calcium content. Then, CML8 and GAD4 are involved in calcium signaling. Yeast two–hybrid assays, firefly luciferase complementation imaging, and GST pull–down assays demonstrated that CML8 interacts with GAD4. Finally, (Z)–3–hexenol treatment increased the GABA contents in Arabidopsis leaves, thus increasing plant resistance to the insect Plutella xylostella. This study revealed the mechanism of activating plant insect defense induced by (Z)–3–hexenol, which is of great significance for the study of volatiles as biological control measures.