Growth is one of the most important traits of an organism. For exploited species, this trait has ecological and evolutionary consequences as well as economical and conservation significance. Rapid changes in growth rate associated with anthropogenic stressors have been reported for several marine fishes, but little is known about the genetic basis of growth traits in teleosts. We used reduced genome representation data and genome-wide association approaches to identify growth-related genetic variation in the commercially, recreationally, and culturally important Australian snapper (Chrysophrys auratus, Sparidae). Based on 17,490 high-quality SNPs and 363 individuals representing extreme growth phenotypes from 15,000 fish of the same age and reared under identical conditions in a sea pen, we identified 100 unique candidates that were annotated to 51 proteins. We documented a complex polygenic nature of growth in the species that included several loci with small effects and a few loci with larger effects. Overall heritability was high (75.7%), reflected in the high accuracy of the genomic prediction for the phenotype (small vs. large). Although the SNPs were distributed across the genome, most candidates (60%) clustered on chromosome 16, which also explains the largest proportion of heritability (16.4%). This study demonstrates that reduced genome representation SNPs and the right bioinformatic tools provide a cost-efficient approach to identify growth-related loci and to describe genomic architectures of complex quantitative traits. Our results help to inform captive aquaculture breeding programmes and are of relevance to monitor growth-related evolutionary shifts in wild populations in response to anthropogenic pressures.