Dichloromethane (DCM; CH2Cl2) is a toxic groundwater pollutant of both natural and anthropogenic origin. DCM is a water immiscible liquid under standard conditions and because of its high specific gravity, when released into the environment sinks vertically through the vadose zone and resides as a dense non-aqueous phase liquid in anoxic groundwater. Quaternary amines (QAs) such as choline, glycine betaine and L-carnitine on the other hand are important dietary compounds found mainly in animal products, they are also marine osmolytes that enable microorganisms to cope with osmotic stress typically found in coastal environments. In the human gut QAs can are metabolized to trimethylamine (TMA) a pro-atherogenic metabolite associated with cardiovascular disease. While in intertidal coastal sediments glycine betaine is a significant precursor to biogenic methane produced in these environments. Here we describe a novel bacterium enriched from ground water near Sydney’s Botany Bay (an area known to traditional custodians of the land as “Warabiya”) that can metabolize both DCM and quaternary amines in novel ways. The bacterium named Ca. Formimonas warabiya (FOWA) can use DCM as a sole source of organic carbon and electrons producing the environmentally benign compound acetate and inorganic chloride. Stable carbon isotope experiments revealed that FOWA assimilated carbon from both DCM and bicarbonate via the Wood-Ljungdhal pathway. Furthermore, FOWA is the first DCM metabolizing organism to shown to use non-chlorinated substrates including: methanol, glycine betaine and choline. FOWA was able to ferment methanol to acetate and demethylate QAs, ultimately producing monomethylamine (MMA) and acetate. MMA is not associated cardiovascular disease and has 66% less methanogenic potential than TMA. The genome of FOWA was sequenced and found to contain 86 nonredundant methyltransferase genes and zero reductive dehalogenases. The ability of FOWA to use different substrates was exploited in differential proteomic experiments to reveal the enzymes and associated genes involved in DCM and glycine betaine metabolism. These experiments revealed the expression of distinct methyltransferase gene cassettes associated with the different substrates applied. The findings of this research significantly increase our understanding of the fate of DCM and glycine betaine in anoxic environments such as those found in the subsurface water, coastal sediments, and the human gut.