In a more than 30 year evolutionary experiment we tested the genomic consequences of hybridisation and selection between fish with different sex chromosome systems. This experiment mimicked an evolutionary scenario, hybridisation with repeated backcrossing, that has likely contributed to the evolution of two freshwater fish species, Xiphophorus clemenciae and X. monticolus. We find that introgression and imposing selection for pigmentation phenotypes on backcrossed individuals results in the retention of an unexpectedly large maternally derived genomic region. Our results show that during the hybridisation process the sex-determining region of the X chromosome from one parental species (the platyfish, X. maculatus) was translocated to an autosome in the hybrids (with X. hellerii) and has led to the evolution of a new sex chromosome, which acts as a W. Our results highlight the complexity of factors contributing to patterns observed in the hybrid genomes, and for the first time experimentally demonstrate that hybridisation can catalyze rapid evolution of genome architecture.