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<i>Aeromonas veronii</i> is widespread in aquatic environments and is responsible for infecting various aquatic animals. In this study, a dominant strain was isolated from the hepatopancreas of diseased <i>Macrobrachium rosenbergii</i> and was named JDM1-1. According to its morphological, physiological, and biochemical characteristics and molecular identification, isolate JDM1-1 was identified as <i>A. veronii</i>. The results of artificial challenge showed isolate JDM1-1 had high pathogenicity to <i>M. rosenbergii</i> with an LD₅₀ value of 8.35 × 10⁵ CFU/mL during the challenge test. Histopathological analysis revealed severe damage in the hepatopancreas and gills of the diseased prawns, characterized by the enlargement of the hepatic tubule lumen and gaps between the tubules as well as clubbing and degeneration observed at the distal end of the gill filament. Eight virulence-related genes, namely <i>aer</i>, <i>ompA</i>, <i>lip</i>, <i>tapA</i>, <i>hlyA</i>, <i>flgA</i>, <i>flgM</i>, and <i>flgN</i>, were screened by PCR assay. In addition, virulence factor detection showed that the JDM1-1 isolate produced lipase, lecithinase, gelatinase, and hemolysin. Furthermore, the mRNA expression profiles of immune-related genes of <i>M. rosenbergii</i> following <i>A. veronii</i> infection, including <i>ALF1</i>, <i>ALF2</i>, <i>Crustin</i>, <i>C-lectin,</i> and <i>Lysozyme,</i> were assessed, and the results revealed a significant upregulation in the hepatopancreas and intestines at different hours post infection. This study demonstrates that <i>A. veronii</i> is a causative agent associated with massive die-offs of <i>M. rosenbergii</i> and contributes valuable insights into the pathogenesis and host defense mechanisms of <i>A. veronii</i> invasion.