Poly(aspartic acid) (PAA) is a green alternative to non-biodegradable poly(carboxylates) and has applications in both industrial and biomedical settings. PAA is synthesized by heating monomeric aspartic acid to yield a polysuccinamide that can be ring-opened to yield thermal PAA composed of 30% α-amide and 70% β-amide linkages. Here, we report the first X-ray crystal structure of a PAA hydrolase from the bacteria Sphingomonas sp. KT-1 (PahZ1KT-1) which functions to degrade synthetic PAA to oligo(aspartic acid) by selective cleavage of β-amide linkages. The structure was solved to 2.45 Å and shows a dimeric assembly where each monomer maintains an α/β hydrolase fold with a prominent, positively lined trough responsible for binding the anionic polymeric substrate. The putative catalytic sites of each monomer lie at the surface of the enzyme on opposite faces. The dimeric interface, as supported by small-angle X-ray scattering/multi-angle light scattering data, is primarily hydrophobic and is further stabilized by flanking hydrogen bonds. Molecular dynamics simulations support the previously determined specific cleavage of only the β-amide linkage through a conformational change that aligns the substrate with the active site Ser. These data provide a scaffold for further understanding the mechanism of PAA hydrolysis and opens the opportunity for using protein engineering to catalyze the biodegradation of other xenobiotics.