The mechanisms of carotenoid accumulation in yellow-fleshed sweetpotato cultivars are unclear. In this study, we compared the transcriptome profiles of a yellow-fleshed cultivar, Beniharuka (BH) and two of its spontaneous white-fleshed mutants (WH2 and WH3) to reveal the genes involved in yellow flesh. As a result of RNA sequencing, a total of 185 differentially expressed genes (DEGs) were commonly detected in WH2 and WH3 compared to BH. Of these genes, 85 DEGs and 100 DEGs were commonly upregulated and downregulated in WH2 and WH3 compared to BH, respectively. g1103.t1, a paralog of zeaxanthin epoxidase (ZEP), was only DEG common to WH2 and WH3 among 38 genes considered to be involved in carotenoid biosynthesis in storage roots. The expression level of g1103.t1 was also considerably lower in five white-fleshed cultivars than in five yellow-fleshed cultivars. Analysis of carotenoid composition in the storage roots showed that the epoxidised carotenoids were drastically reduced in both WH2 and WH3. Therefore, we propose that the ZEP paralog, g1103.t1, may be involved in carotenoid accumulation through the epoxidation of β-carotene and β-cryptoxanthin in sweetpotato.