The body wall is the main edible part of the sea cucumber (Apostichopus japonicus). The body wall proportion (the proportion of body wall weight to total weight, BWP) is an important economic trait and acts as an important indicator for assessing the quality of sea cucumber. Studying the genetic regulatory mechanisms of BWP can provide a scientific basis for sea cucumber breeding. To screen for candidate functional genes and molecular markers related to BWP, 250 randomly selected sea cucumber individuals from the same breeding batch and in the same culture environment were used to measure individual body wall proportions. After sorting by BWP, the top 10% (25 individuals) with the highest BWP and the bottom 10% (25 individuals) with the lowest BWP were assigned to the H and L groups, respectively. Using whole-genome resequencing and selection sweep analysis, the selected regions were screened, genes and key pathways were excavated, and single nucleotide polymorphism (SNP) loci and dominant genotypes related to BWP were determined. A total of 7398410 high-quality SNPs were obtained from the whole-genome sequencing. Analysis of the population genetic structure showed no obvious difference in genetic structure between the two groups. Based on the selection sweep analysis of Fst and Pi, 524 and 484 selection regions were screened in the high and low BWP groups, respectively, and annotated to 214 and 193 candidate functional genes, respectively. Pathway enrichment analysis obtained 1199 predicted GO categories and 44 KEGG metabolic pathways, among which four significantly differentially enriched pathways related to BWP were identified: metabolic pathways, fatty acid elongation, fatty acid metabolism, and mucin-type O-glycan biosynthesis. Through retrieval and analysis of functional genes, five functional genes possibly related to high BWP, ELP2, TPRA1, G2E3, TIE1, and DOCK1, were screened. Furthermore, 28 SNP loci within these five related genes were screened and four dominant genotypes related to BWP were obtained. The results provide basic data for exploring the genetic regulation mechanism of the BWP of Apostichopus japonicus and lay a foundation for the development of molecular-assisted selection technology and genomic breeding chips. Relevant research results also provide a basis for the selective breeding of high-quality Apostichopus japonicus varieties.