Genetic sexing strains (GSS) used in sterile insect technique (SIT) programs are textbook examples of how classical Mendelian genetics can be directly implemented in the management of agricultural insect pests. Though the foundation of traditionally developed GSS are single locus, autosomal recessive traits, their genetic basis are largely unknown. With the advent of modern genomic techniques, the genetic basis of sexing traits in GSS can now be further investigated. This study is the first of its kind to integrate traditional genetic techniques with emerging genomics to characterize a GSS using the tephritid fruit fly pest Bactrocera cucurbitae as a model. These techniques include: whole genome sequencing, the development of a mapping population, linkage map and quantitative trait analysis. The experiment designed to map the genetic sexing trait in B. cucurbitae, wp, also enabled the generation of a chromosome-scale genome assembly by integrating the linkage map with the assembly. Quantitative trait loci analysis revealed SNP loci near position 42 MB on chromosome 3 to be tightly linked to wp Gene annotation and synteny analysis show a near-perfect relationship between chromosomes in B. cucurbitae and Muller Elements A-E in Drosophila melanogaster This chromosome-scale genome assembly is complete, has high contiguity, was generated using a minimal input DNA, and will be used to further characterize the genetic mechanisms underlying wp Knowledge of the genetic basis of genetic sexing traits can be used to improve SIT in this species and expand to other economically important Diptera.