The plasmid-mediated mcr-9 gene has been widely detected in Salmonella across multiple countries and regions, raising significant concerns for food safety and public health. To investigate the transmission dynamics of mcr-9 in Salmonella, we conducted a comprehensive genomic epidemiological study and explored the potential mechanisms of mcr-9 transmission in poultry-derived S. Thompson in China. This study analyzed 126 mcr-9-positive Salmonella isolates from food in China and genomic data of 1,487 publicly available mcr-9-positive Salmonella collected over the past 40 years from 32 countries and various sources. Two variants, mcr-9.1 and mcr-9.2, were detected, with mcr-9.1 being the most prevalent subtype globally. S. Typhimurium/I 4,[5],12:i:- (23.1 %, 372/1,613) was the dominant lineage of the total collection, followed by S. Saintpaul (15.9 %, 256/1,613), S. Heidelberg (11.4 %, 184/1,613), and S. Thompson (8.6 %, 139/1,613). S. Typhimurium/I 4,[5],12:i:- was widely distributed in North America and Europe, primarily prevalent in humans and swine, whereas S. Thompson was predominantly found in China, mainly prevalent in poultry-related foods and humans. Conjugation experiments were performed on 116 S. Thompson strains from 126 Salmonella isolates. The results showed that 85.3 % (99/116) of the mcr-9-positive plasmids were transferable. The IncHI2-IncHI2A plasmids from three representative donors demonstrated the ability to transfer at varying frequencies to seven Salmonella recipients of different serotypes including Typhimurium, Thompson, Enteritidis, Indiana, Rissen, London, and Derby. Chicken juice matrix significantly increased the proportion of mcr-9-positive S. Thompson conjugants. The inability of mcr-9-positive IncHI2-IncHI2A plasmids to transfer via conjugation may be due to the integration of the plasmid into the chromosome. In addition, the deletion of IS1B-cfdB-fucO-frmR-uvrA-fghA-gloA-frmA-uvrB-flhD-smc-copG-IS26 gene region was observed in the non-conjugative mcr-9-positive plasmids. These findings underscore the importance of ongoing surveillance of mcr-9-positive multidrug-resistant S. Thompson for food safety in China.