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SUMMARY: Nucleolar dominance (ND) is a widespread epigenetic phenomenon in hybridizations where nucleolus transcription fails at the nucleolus organizer region (NOR). However, the dynamics of NORs during the formation of Triticum zhukovskyi (GGAuAuAmAm), another evolutionary branch of allohexaploid wheat, remains poorly understood. Here, we elucidated genetic and epigenetic changes occurring at the NOR loci within the Am, G, and D subgenomes during allopolyploidization by synthesizing hexaploid wheat GGAuAuAmAm and GGAuAuDD. In T. zhukovskyi, Au genome NORs from T. timopheevii (GGAuAu) were lost, while the second incoming NORs from T. monococcum (Am Am) were retained. Analysis of the synthesized T. zhukovskyi revealed that rRNA genes from the Am genome were silenced in F1 hybrids (GAuAm) and remained inactive after genome doubling and subsequent self‐pollinations. We observed increased DNA methylation accompanying the inactivation of NORs in the Am genome and found that silencing of NORs in the S1 generation could be reversed by a cytidine methylase inhibitor. Our findings provide insights into the ND process during the evolutionary period of T. zhukovskyi and highlight that inactive rDNA units may serve as a 'first reserve' in the form of R‐loops, contributing to the successful evolution of T. zhukovskyi. Significance Statement: Nucleolar dominance is a widespread epigenetic phenomenon in distant hybridizations, which describes reversible nucleolus transcription failure at the uniparental NOR. Triticum zhukovskyi lost Au genome NORs during the first polyploidization event, but retained Am genome NORs across the second polyploidization process. Nucleolus dominance is established in hybrid F1 independently of chromosome doubling events, which may be one of the reasons for the successful evolution of hexaploid wheat T. zhukovskyi. [ABSTRACT FROM AUTHOR]