Burkholderia pseudomallei is the causative agent of the high-mortality disease melioidosis. Although melioidosis is classified as a tropical disease, rare autochthonous cases have been reported from temperate climatic regions, with uncertainty as to whether B. pseudomallei is persistent in the local environment and whether specific genetic mechanisms facilitate the survival of B. pseudomallei outside the tropics. Sporadic cases of melioidosis occurred in a valley region (latitude 31.6°S) in southwest Western Australia, Australia, between 1966 and 1992. We report a new melioidosis cluster in the same region following high rainfall in January 2017. More than 20 animals died, and B. pseudomallei was isolated from four alpacas, a parrot, and three environmental samples taken from the farm where the alpacas resided. Epidemiological data and genomics revealed that two locations on the farm were the probable sources of the alpaca infections. We determined that B. pseudomallei isolates from the 2017 cluster belonged to sequence type 284 (ST-284), as did all isolates recovered from 1966 to 1992. Genomic analysis confirmed that the ST-284 isolates were clonal and contained conserved genomic islands and limited evidence of recombination. We identified protein-coding regions unique to these isolates that might influence the persistence of B. pseudomallei in this temperate region. We demonstrate the environmental persistence of B. pseudomallei in a temperate region for over 50 years, with limited genetic changes suggesting a latent state and with activation, potential aerosolization, and local dispersal following unusually high rainfall.