Several mutations of the sorghum [Sorghum bicolor (L.) Moench] GRANULE-BOUND STARCH SYNTHASE (GBSS) gene [Sobic.010G022600] result in a low amylose:amylopectin starch ratio in the endosperm and confer a glutinous, “waxy” texture; hence, the wild-type gene is commonly referred to as Waxy (Wx). Recessive waxy (wx) alleles improve starch digestibility in ethanol production, human foods and beverages, and animal feed. However, breeding waxy sorghum can be time-consuming due to the need for grain to reach physiological maturity before the trait can be phenotyped and ongoing reliance on PCR markers for genotyping, which are not amenable to next-generation sequencing (NGS). Modern genomics-assisted breeding requires conducing high-throughput genotyping and selection in large, segregating populations prior to flowering. This study provides the first published NGS markers for the two mostly commonly used waxy (wx) alleles of sorghum and is the first to fully characterize the large insertion that is causal of the wxa allele. An enhanced genome assembly was constructed from the B.Tx623 reference genome (v3.1.1) to include the 5.6 kb large retrotransposon derivative (LARD) in the wxa allele. This improved read mapping at Sobic.010G022600 in wxa individuals, identified 78 new uniquely mapped reads, and made it possible to distinguish different Waxy genotypes using short-read sequencing data. Functional PACE-PCR markers, suitable for genomic selection, were developed for Wx, wxa, and wxb alleles and validated in three public and private breeding programs. These new molecular breeding resources will improve the efficiency of developing commercial waxy sorghum hybrids.