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The marine pathogen Vibrio alginolyticus employs its type III secretion system (T3SS), a syringe-like secretion apparatus, to kill eukaryotic cells. Although the cascade regulation of the ExsACDE operon has been described in detail for the V. alginolyticus T3SS, little is known about the signals and signaling pathways that regulate the operon. Herein we determined that the hybrid sensor kinase ArcB forms a signaling cascade with core members of the quorum sensing (QS) system (LuxU and LuxO) to regulate the expression of the V. alginolyticus T3SS. We further show that ArcB initiates the cascade by functioning as a sensor protein for bacterial autoinducer-2 (AI-2), a signaling molecule used for inter-species communication. In addition, we demonstrate that host cells produce an AI-2 mimic during the infection stage, which can also be sensed by ArcB and can activate the gene expression of T3SS.