cis-Dichloroethene (cDCE) and vinyl chloride (VC) in groundwater migrating through the oxic/anoxic interface (OAI) of freshwater sediment can be degraded by anaerobic reductive dechlorination, aerobic (co)metabolic degradation or combination of both. We tested this using microcosms prepared from OAI sediment samples incubated under varying oxic/anoxic incubations. In microcosms containing low organic carbon sediment, oxygen exposure resulted in substantial decay of strictly anaerobic Dehalococcoides mccartyi (Dcm) and impaired its resilience under subsequent anoxic conditions. VC was metabolically oxidized in these microcosms the sediment of which had the history of exposure to high VC concentration reaching OAI at the site. However, no metabolic aerobic cDCE degradation was found. In contrast, in microcosms with high organic carbon sediment, Dcm seemed protected against oxygen, reductively dechlorinating cDCE/VC-to-ethene and subsequent ethene-to-CO2 oxidation by ethenotrophs. The apparent lack of mass balance might be mischaracterized as metabolic cDCE/VC oxidation. Dcm showed an unrecognized resilience against oxygen toxicity in these microcosms the sediment of which were characterized with historically active reductive dechlorination and negligible VC reaching OAI. Our results imply prolonged VC exposure as a prerequisite for evolution of VC-oxidizers from ethene-oxidizers. However, MiSeq sequencing of partial etnE gene involved in VC/ethene aerobic degradation did not reveal sequence divergence responsible for VC-oxidation vs ethene-oxidation lifestyle.