Cyprinids, the largest and most economically significant family of teleosts, comprise over 600 polyploid species, whose genomic complexity presents challenges in deciphering the genetic basis of phenotypic diversity. In this study, we generated high-quality haplotype-resolved genomes for two representative Cyprinidae allopolyploids (Cyprinus rubrofuscus and Sinocyclocheilus grahami) by constructing the diploid genome of their hybrid (C. rubrofuscus ♀ × S. grahami ♂, CRSG). The haplotype assembly for C. rubrofuscus contained 50 chromosomes (1.5 Gb, scaffold N50 = 29.64 Mb), while S. grahami contained 48 chromosomes (1.8 Gb, scaffold N50 = 36.04 Mb). Genomic analyses refined the ancestral divergence times and provided new insights into chromosomal fusion events, gene family expansions and contractions, and positively selected genes driving phenotypic divergence between the two species. Comparative analysis of economic traits and gene expression in C. rubrofuscus, S. grahami, and their reciprocal hybrids identified several key genes associated with enhanced growth (e.g., OXPHOS-related genes), optimized fatty acid composition (e.g., tecr, acot1, acsl1, cpt2), and hybrid sterility (e.g., cyp19a1, wt1, dmrtb1). Notably, parental haplotype dominance of those genes were observed, haplotype genes derived from C. rubrofuscus (CR-Hg) predominantly contributed to the accelerated growth of reciprocal hybrids, exhibiting significantly higher expression levels of OXPHOS-related genes compared to those derived from S. grahami (SG-Hg). Conversely, SG-Hg played a central role in optimizing fatty acid composition in CRSG, with genes involved in polyunsaturated fatty acid biosynthesis and degradation showing markedly higher expression levels than their CR-Hg counterparts. Parental haplotype genes both regulated the sterility of CRSG, as no significant differences were observed between CR-Hg and SG-Hg in the sex differentiation and meiotic disorder-related genes. This study highlight the potential of C. rubrofuscus and S. grahami as genetic resources for developing hybrids with improved growth rates and optimized fatty acid profiles, provide valuable genomic resources and theoretical insights for aquaculture breeding.