Since it was first imported into Vietnam in the 2000s, the pompano fish (Trachinotus blochii) has gained popularity as a good candidate for mariculture systems. Between 2010 and 2014, however, several outbreaks of nocardiosis attributed to Nocardia seriolae caused massive fish mortalities in pompano farms throughout the country. Based on phenotypic and biochemical properties, 55 strains of N. seriolae were isolated from infected pompano in four central Vietnamese provinces. To further understand the origin, evolution and epidemiology of the pathogen, six strains from all provinces were randomly selected and tested for their genetic relatedness using pulsed-field gel electrophoresis (PFGE) and Illumina NextSeq 500 whole genome sequencing (WGS). PFGE with XbaI and AseI digestions revealed two pulsotypes with a similarity of > 80%, suggesting close genetic relatedness of these strains. Consistent with PFGE, phylogenomic analysis of the above seven Vietnamese strains and all currently available N. seriolae genomes (n=7) using whole-genome-derived single-nucleotide polymorphisms (SNPs) indicated that all seven strains fall into a single clade containing two highly clonal genotypes that differed by just 102 SNPs, irrespective of the geographic regions where they were isolated. The Vietnamese strains share a common ancestor with strains isolated from other countries in the same region, although they differed from the next closest known strain by at least 265 SNPs. These results suggest that the Vietnamese N. seriolae strains have been recently introduced to this country, although the precise origin is not yet known. The bacterium encodes a large genome of 7,785,433 bp, a G + C content of 68.2%, 7,420 predicted coding DNA sequences and 77 transfer RNA sequences. It was also found that the bacterium harboured genes coding for virulence factors such as iron uptake systems, resistance to antibiotics and toxic compounds, the biosynthesis of lipid and protein, hemolysins, adhesins and proteases. These findings help focus our future targets for vaccine development against Nocardia in the aquaculture sector and more generally provide novel information about the Vietnamese N. seriolae population.