The plant genome is partitioned across three distinct cellular compartments: the nucleus, mitochondria, and chloroplasts. Interactions between nuclear-encoded gene products and those of cytoplasmic genomes (i.e., cytonuclear interactions) underlie the essential cellular processes such as respiration and photosynthesis. Whole genome duplication events (WGDs) are a prominent process of diversification in eukaryotes and are expected to perturb cytonuclear interactions in two fundamental ways: altering the genetic stoichiometry of cytonuclear interactions and increasing cell size. Organelle size, organelle genome copy numbers, cytonuclear transcriptomic and proteomic stoichiometry, and ultimately the efficiency of carbon fixation and ATP production might all be altered as a consequence of WGD, but many decades of careful investigation into polyploidy have yet to fully evaluate these predictions. We investigated the relationship between nuclear and organelle genome copy numbers in common-garden reared diploid and polyploid accessions of both wheat and Arabidopsis. Our droplet digital PCR (ddPCR) estimates of nuclear, mitochondrial, and chloroplast genome copy numbers revealed evidence of substantial intra-specific and intra-individual variation for organelle genome copy number, as well as evidence that polyploids exhibit elevated organelle genome copy numbers per cell. Taken together, our results indicate that polyploids appear to compensate for increased nuclear genome content with increased organelle genome copies in both monocots and dicots, indicating that cytonuclear stoichiometry is an important component of successful interactions between nuclear and cytoplasmic genomes.