Enhanced biological phosphorus removal (EBPR) is an important industrial wastewater treatment process mediated by polyphosphate-accumulating organisms (PAOs). Members of the genus Candidatus Accumulibacter are one of the most extensively studied PAO as they are commonly enriched in lab-scale EBPR reactors. Members of different Accumulibacter clades are often enriched through changes in reactor process conditions; however, the two currently sequenced Accumulibacter genomes show extensive metabolic similarity. Here, we expand our understanding of Accumulibacter genomic diversity through recovery of eight population genomes using deep metagenomics, including seven from phylogenetic clades with no previously sequenced representative. Comparative genomic analysis revealed a core of shared genes involved primarily in carbon and phosphorus metabolism; however, each Accumulibacter genome also encoded a substantial number of unique genes (>700 genes). A major difference between the Accumulibacter clades was the type of nitrate reductase encoded and the capacity to perform subsequent steps in denitrification. The Accumulibacter clade IIF genomes also contained acetaldehyde dehydrogenase that may allow ethanol to be used as carbon source. These differences in metabolism between Accumulibacter genomes provide a molecular basis for niche differentiation observed in lab-scale reactors and may offer new opportunities for process optimization.