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Oryza australiensis (EE genome), the sole representative of the EE genome in the genus, holds significant value for deciphering polyploid evolution and mining stress-resistance genes owing to its extreme environmental adaptability. Here, we report a telomere-to-telomere (T2T) genome assembly of O. australiensis, yielding a 901 Mb genome with 12 complete chromosomes. This enables comprehensive annotation of centromeres, telomeres, and 36,742 genes, revealing non-canonical telomeric repeats and three distinct centromere repositioning mechanisms: inversion-driven shifts, duplication-mediated neocentromerization, and transposon burst-induced neocentromere formation. Crucially, transposon dynamics analysis reveals synchronized amplification of Angela LTR retrotransposons in the EE genome and the DD subgenome of allotetraploid O. alta (CCDD) prior to CCDD formation. Phylogenetic and synteny analyses of Angela LTR integrase domains, alongside a 275-bp repeat marker exclusive to EE and DD, indicate that the ancestral lineage that contributed the DD subgenome share common ancestry with an EE-like progenitor. These findings refine Oryza evolutionary history and highlight transposon dynamics in reconstructing deep evolutionary relationships.