Color is a crucial component of the commercial value of citrus fruits. Carotenoid cleavage oxygenases (CCOs) can affect fruit color by oxidative cleavage of different carotenoid sites, resulting in various colors. This study proposed a genome-wide analysis of the Orah mandarin CCO gene family using bioinformatics methods and combined physiological, transcriptomic, and metabolomic data to analyze the gene expression levels and carotenoid accumulation mechanisms of different colored peel. A total of 14 CCOs were identified in the Orah mandarin genome. Phylogenetic analysis revealed that CrCCOs can be classified into six subfamilies, and the gene structure and conserved motifs support the above classification. GO and KEGG functional annotation revealed that Orah mandarin CCO genes play crucial roles in carotenoid synthesis and catabolism. Transcriptomic data showed that the expression level of CrCCD4b1 was positively correlated with the current status of Orah mandarin red flavedo. Physiological and metabolomic studies further revealed that apocarotenal and β-citraurin were identified as the key metabolites controlling the change in flavedo color from yellow to red. Correlation analysis revealed CrCCD4b1 as a crucial gene in the apocarotenal and β-citraurin expression network. For the first time, we proposed CrCCD4b1 as a potential model for increasing red carotenoid accumulation in the flavedo by promoting the biosynthesis of C30 carotenoids (apocarotenal, β-citraurin) in Orah mandarin. This study will lay the foundation for further research on the causes of differences in peel color and the mining of crucial genes regulating the red trait.