It has previously been found that CaWRKY40 is employed by pepper to activate immunity against Ralstonia solanacearum and to activate thermotolerance context-specifically, but the underlying mechanisms are not fully understood. Here, CaGβ, a subunit in the heterotrimeric G protein complex that was originally found to probably interact with CaWRKY40, was expressional and functionally characterized; the results showed that CaGβ was upregulated by R. solanacearum infection; its silencing by virus-induced silencing impaired pepper immunity against R. solanacearum infection, accompanied by downregulation of immunity-related marker genes, including CaPR1, CaDEF1, CaNPR1, and CaPR-STH2. In addition, CaGβ–CaWRKY40 interaction was confirmed by BiFC and pull-down assay using prokaryotically expressed proteins, and activations of immunity-related CaPR1, CaPR-STH2, and CaNPR1 by CaWRKY40 were all promoted, but the activation of thermotolerance-related CaHSP24 by CaWRKY40 blocked CaGβ through its interaction with CaWRKY40. All these data indicate that immunity against R. solanacearum and its antagonism to thermotolerance in pathogen-infected pepper plants are mediated by CaWRKY40 through physical interaction with CaGβ.