In August and September 2022, two disease outbreaks were observed in Kuruma shrimp (Penaeus japonicus) farms in Okinawa, Japan. Diseased animals exhibited clinical signs of whitened musculature extending from the abdominal to the distal region. Histopathology revealed degeneration of fibers due to liquified muscle necrosis and haemocytic infiltration. Analysis of nonhost contigs from the assembled unmapped RNA and DNA shotgun sequence reads showed significant taxonomic alignment to bacterial species. This led to the investigation of a bacterium as a possible causative agent by characterizing its population in the diseased shrimp muscle. The majority of the 16S rRNA sequence recombinant clones had their highest homology with Photobacterium sp. (> 99%). The three bacterial isolates from the whitened muscle tissue were identified as Photobacterium damselae subsp. damselae (WMD-P1, WMD-P2 and WMD-P3) by biochemical and molecular assays and were further characterized. The Pdd genomes consisted of two circular chromosomes with varying numbers of plasmid. Its size ranges from 4.47 Mb to 4.60 Mb with an average GC content of 40.8%, with predicted number of coding sequences (CDs) ranging from 3816 to 4031. hlyA and pldA genes encoding for leukocidin pore-forming toxin and phospholipase were identified. Putative virulence genes are involved in adherence, antiphagocytosis, chemotaxis and motility, iron uptake, quorum sensing, secretion system, and immune evasion. The presence of prophages, genomic islands and antimicrobial resistant genes in the Pdd genomes suggests episodes of horizontal gene transfer. Average nucleotide identity (ANI) and pangenome analyses revealed a high genetic relationship of the Pdd strains (>98%) to isolates from other sources. PCR assays validated the presence of two bacterial virulence genes encoding the pore-forming toxin and phospholipase respectively in all isolates. Also, the strains had chitinase, phospholipase, and hemolytic activities. Intramuscular injection at 1 × 108 CFU/ml bacterial concentration produced pathological signs similar to those in naturally infected shrimp after 24 hpi. Lower concentration of 1 × 103 CFU/ml resulted in morbidity after 10 dpi. These results show that P. damselae subsp. damselae (Pdd) is associated with the occurrence of white muscle disease in Kuruma shrimp.