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SUMMARY Plants rely on tight coordination between nuclear, mitochondrial, and chloroplast genomes to form essential multi‐enzyme cytonuclear complexes. Whole‐genome duplication (WGD) doubles the nuclear genome, potentially disrupting cytonuclear stoichiometry unless organellar genomes respond accordingly. Targeted analyses of chloroplasts and mitochondria enabled us to dissect the extent and mechanisms of adjustments in both organelles immediately after WGD and across generations in Arabidopsis auto‐ and allopolyploids. We observed a substantial overcompensation of organellar genome copies in both organelles in early‐generation autotetraploids primarily through multiplication of DNA copies within organelles rather than increasing the number of organelles. Despite higher DNA content, mitochondria maintained their volume, and chloroplasts were even smaller. In successive generations, chloroplast DNA copy numbers continued to rise, whereas mitochondrial DNA copies declined. Gene expression patterns also differed between chloroplasts and mitochondria and between auto‐ and allopolyploids. In autopolyploids, immediate transcriptional changes were minimal, but by the fourth generation after WGD, nuclear genes involved in mitochondria‐nuclear complexes were downregulated. In allopolyploids, transcriptional changes appeared immediately in the first generation (chloroplast genes were upregulated and mitochondrial genes were downregulated). Our findings demonstrate that cytonuclear balance is restored through dynamic, organelle‐specific, and polyploid‐type‐specific mechanisms. These insights advance our understanding of the evolution of polyploid genomes.