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Summary Genome merging is a common phenomenon causing a wide range of consequences on phenotype, adaptation, and gene expression, yet its broader implications are not well‐understood. Two consequences of genome merging on gene expression remain particularly poorly understood: dosage effects and evolution of expression.We employedChlamydomonas reinhardtiias a model to investigate the effects of asymmetric genome merging by crossing a diploid with a haploid strain to create a novel triploid line. Five independent clonal lineages derived from this triploid line were evolved for 425 asexual generations in a laboratory natural selection experiment.Utilizing fitness assays, flow cytometry, and RNA‐Seq, we assessed the immediate consequences of genome merging and subsequent evolution. Our findings reveal substantial alterations in genome size, gene expression, protein homeostasis, and cytonuclear stoichiometry. Gene expression exhibited expression‐level dominance and transgressivity (i.e. expression level higher or lower than either parent). Ongoing expression‐level dominance and a pattern of ‘functional dominance’ from the haploid parent was observed.Despite major genomic and nucleo‐cytoplasmic disruptions, enhanced fitness was detected in the triploid strain. By comparing gene expression across generations, our results indicate that proteostasis restoration is a critical component of rapid adaptation following genome merging inChlamydomonas reinhardtiiand possibly other systems.