Genome-resolved insights into the structure and function of the drinking water microbiome can advance the effective management of drinking water quality. To enable this, we constructed and curated thousands of metagenome-assembled and isolate genomes from drinking water distribution systems globally to develop a Drinking Water Genome Catalog (DWGC). The current DWGC disproportionately represents disinfected drinking water systems due to a paucity of metagenomes from nondisinfected systems. Using the DWGC, we identify core genera of the drinking water microbiome including a genus (UBA4765) within the order Rhizobiales that is frequently detected and highly abundant in disinfected drinking water systems. We demonstrate that this genus has been widely detected but incorrectly classified in previous amplicon sequencing-based investigations of the drinking water microbiome. Further, we show that a single genome variant (genomovar) within this genus is detected in 75% of drinking water systems included in this study. We propose a name for this uncultured bacterium as “Raskinella chloraquaticus” and describe the genus as “Raskinella” (endorsed by SeqCode). Metabolic annotation and modeling-based predictions indicate that this bacterium is capable of necrotrophic growth, is able to metabolize halogenated compounds, proliferates in a biofilm-based environment, and shows clear indications of disinfection-mediated selection.