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Commonly used flame retardants, such as polybrominated diphenyl ethers, are extremely persistent in the environment, causing serious environmental risks. Certain strains of bacteria are able to degrade several low brominated congeners of PBDEs aerobically. However, the aerobic degradation pathway is not yet well understood, particularly at the genetic level. In this study, we isolated Cupriavidus sp. WS from the environment that could degrade diphenyl ether (DE), 4-bromodiphenyl ether, and 4,4'-bromodiphenyl ether. DE was completely degraded in 6 days without any detectable end-product. Using transposon mutagenesis, several DE degradation-deficient mutants were obtained. Knocking out bphA1, bphA2, and bphA3 eliminated the ability of the Cupriavidus sp. WS bacterium to degrade DE, indicating that the bph genes play a crucial role in DE degradation by this strain. The specific roles of bphA, bphB, and bphC were identified by systematically expressing these genes in Escherichia coli. The dihydrodiol product of BphA was dehydrogenated into 2,3-dihydroxydiphenyl ether by BphB. 2,3-Dihydroxydiphenyl ether was then decomposed into phenol and 2-pyrone-6-carboxylic acid by BphC. Thus, BphA, BphB, and BphC act sequentially in the aerobic degradation of DE, 4-bromodiphenyl ether, and 4,4'-dibromodiphenyl ether by the Cupriavidus sp. WS bacterium.