Carbapenem-resistant (CRE) are a serious public health threat because of their rapid dissemination. To determine the epidemiological and genetic characteristics of CRE infections in Thailand, we performed whole-genome sequencing of 577 carbapenem-resistant isolates and 170 carbapenem-resistant isolates from hospitals across the nation. The four most prevalent carbapenemase genes harboured by these bacteria were , , and . The gene was identified in diverse sequence types. The gene was identified almost exclusively in . The genes , , and co-carriage of and were found in specific sequence types from certain provinces. Replicon typing revealed the diverse backbones of - and -harbouring plasmids and successful expansion of -harbouring IncN2-type plasmids. Core-genome single-nucleotide polymorphism analysis suggested that -, -, -, and co-carriage of and -associated sub-clonal lineages have recently predominated in the provinces from where these isolates were isolated. Thus, we demonstrate genotype-dependent dissemination of CRE in Thailand, which is helpful for establishing infection-control strategies in CRE-endemic areas.