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Chlamydia psittaci is a globally distributed veterinary pathogen with zoonotic potential. Although C. psittaci infections have been reported in various hosts, isolation and culture of Chlamydia is challenging, hampering efforts to produce contemporary global C. psittaci genomes. This is particularly evident in the lack of avian C. psittaci genomes from Australia and New Zealand. In this study, we used culture-independent probe-based whole-genome sequencing to expand the global C. psittaci genome catalogue. Here, we provide new C. psittaci genomes from two pigeons, six psittacines, and novel hosts such as the Australian bustard ( Ardeotis australis ) and sooty shearwater ( Ardenna grisea ) from Australia and New Zealand. We also evaluated C. psittaci genetic diversity using multilocus sequence typing (MLST) and major outer membrane protein ( omp A) genotyping on additional C. psittaci -positive samples from various captive avian hosts and field isolates from Australasia. We showed that the first C. psittaci genomes sequenced from New Zealand parrots and pigeons belong to the clonal sequence type (ST)24 and diverse 'pigeon-type' ST27 clade, respectively. Australian parrot-derived strains also clustered in the ST24 group, whereas the novel ST332 strain from the Australian bustard clustered in a genetically diverse clade of strains from a fulmar, parrot, and livestock. MLST and omp A genotyping revealed ST24/ omp A genotype A in wild and captive parrots and a sooty shearwater, whilst 'pigeon-types' (ST27/35 and omp A genotypes B/E) were found in pigeons and other atypical hosts, such as captive parrots, a little blue penguin/Kororā ( Eudyptula minor ) and a zebra finch ( Taeniopygia guttata castanotis ) from Australia and New Zealand. This study provides new insights into the global phylogenomic diversity of C. psittaci and further demonstrates the multi-host generalist capacity of this pathogen.