The genetic mechanisms underlying hybridization are poorly understood despite their potentially important roles in speciation processes, adaptative evolution, and agronomical innovation. In this study, transcription profiles were compared among three populations of brook charr and their hybrids using microarrays to assess the influence of hybrid origin on modes of transcription regulation inheritance and on the mechanisms underlying growth. We found that twice as many transcripts were differently expressed between the domestic population and the two wild populations (Rupert and Laval) than between wild ones, despite their deeper genetic distance. This could reflect the consequence of artificial selection during domestication. We detected that hybrids exhibited strikingly different patterns of mode of transcription regulation, being mostly additive (94%) for domestic × Rupert, and nonadditive for Laval × domestic (45.7%) and Rupert × Laval hybrids (37.5%). Both heterosis and outbreeding depression for growth were observed among the crosses. Our results indicated that prevalence of dominance in transcription regulation seems related to growth heterosis, while prevalence of transgressive transcription regulation may be more related to outbreeding depression. Our study clearly shows, for the first time in vertebrates, that the consequences of hybridization on both the transcriptome level and the phenotype are highly dependent on the specific genetic architectures of crossed populations and therefore hardly predictable.