Fish mortality caused by Streptococcus iniae is a major economic problem for fish aquaculture in warm and temperate regions globally. There is also risk of zoonotic infection by S. iniae through handling of contaminated fish. To date, a handful of complete genomes have been described but our understanding of the genomic diversity of this species is limited. Here we investigated the role of mobile genetic elements (MGEs) in the evolution of S. iniae. We first established a high-quality reference sequence by manually curating the MGEs in a complete reference genome of S. iniae (determined by PacBio long-read sequencing). The reference genome harbours 93 individual insertion sequence (IS) elements comprising 13 different types. We then used the Illumina sequencing to determine the draft genomes of a global collection of 112 S. iniae isolates from different hosts. A non-recombinant core genome maximum likelihood phylogenetic tree revealed separate clustering of human and fish isolates, as well as phylogeographic groupings, even within Australia. By analysing IS distribution across the entire phylogeny we discovered clade-specific expansion of certain IS types. For example, up to 17 additional insertions of an ISSag3-like element were identified in one clade compared to its nearest phylogenetic neighbour. Remarkably, we found several cases of convergent evolution driven by IS, including multiple lineages in which the CRISPR/Cas system had been independently disrupted by different IS types. By defining the role of MGEs in S. iniae diversity we have enabled a better understanding of its evolutionary trajectory and mechanisms of adaptation to different niches.