Models on hybrid speciation assume that hybridization generates increased phenotypic variance that is utilized to invade new adaptive peaks. We test to what extent this prediction can be traced using gene expression data in the fish species Cottus perifretum and Cottus rhenanus as well as a natural hybrid lineage referred to as invasive sculpins. In addition, interspecies crosses were used to explore evolutionary trajectories from initial stages to the hybrid lineage. EST (expressed sequence tag) libraries were sequenced to design an oligonucleotide microarray that was calibrated for probe-specific differences in binding behaviour. Levels of gene expression divergence between species correlate with genetic divergence at neutral markers and, accordingly, invasive sculpins were intermediate between the parental species overall. However, the hybrid lineage is distinguished through unique patterns of gene expression that are enriched for biological functions which represent candidates for the fitness properties of invasive sculpins. We compare F2 crosses with natural invasive sculpins to show that the variance in gene expression decreases in invasives. Moreover, few of the transgressive patterns of gene expression that distinguish invasives can be directly observed in F2 crosses. This suggests that the invasive transcriptome was subject to secondary changes after admixture. The result is in line with an evolutionary process that reduces maladaptive variance and optimizes the phenotype of an emerging hybrid lineage.