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<i>Vibrio parahaemolyticus</i> can cause acute gastroenteritis, wound infections, and septicemia in humans. The overuse of antibiotics in aquaculture may lead to a high incidence of the multidrug-resistant (MDR) pathogen. Nevertheless, the genome evolution of <i>V. parahaemolyticus</i> in aquatic animals and the mechanism of its antibiotic tolerance remain to be further deciphered. Here, we investigated the molecular basis of the antibiotic tolerance of <i>V. parahaemolyticus</i> isolates (<i>n</i> = 3) originated from shellfish and crustaceans using comparative genomic and transcriptomic analyses. The genome sequences of the <i>V. parahaemolyticus</i> isolates were determined (5.0–5.3 Mb), and they contained 4709–5610 predicted protein-encoding genes, of which 823–1099 genes were of unknown functions. Comparative genomic analyses revealed a number of mobile genetic elements (MGEs, <i>n</i> = 69), antibiotic resistance-related genes (<i>n</i> = 7–9), and heavy metal tolerance-related genes (<i>n</i> = 2–4). The <i>V. parahaemolyticus</i> isolates were resistant to sub-lethal concentrations (sub-LCs) of ampicillin (AMP, 512 μg/mL), kanamycin (KAN, 64 μg/mL), and streptomycin (STR, 16 μg/mL) (<i>p</i> < 0.05). Comparative transcriptomic analyses revealed that there were significantly altered metabolic pathways elicited by the sub-LCs of the antibiotics (<i>p</i> < 0.05), suggesting the existence of multiple strategies for antibiotic tolerance in <i>V. parahaemolyticus</i>. The results of this study enriched the <i>V. parahaemolyticus</i> genome database and should be useful for controlling the MDR pathogen worldwide.