The production of capsular polysaccharides by Klebsiella pneumoniae protects the bacterial cell from harmful environmental factors such as antimicrobial compounds and infection by bacteriophages. To bypass this protective barrier, some phages encode polysaccharide degrading enzymes referred to as depolymerases to provide access to cell surface receptors. Here we characterized the bacteriophage RAD2, that infects K. pneumoniae strains that produce the widespread, hypervirulence-associated K2-type capsular polysaccharide. Using Transposon Directed Insertion Sequencing, we show that the production of capsule is an absolute requirement for RAD2 infection. That is, the capsule serves as a first-stage receptor. We have identified the depolymerase (DpK2) responsible for recognition and degradation of the capsule, determined that DpK2 forms globular appendages of the phage virion tail-tip and present the cryo-electron microscopy structure of the depolymerase at 2.7Å resolution. A putative active site for the enzyme was identified, comprising of clustered negatively charged residues that could facilitate the hydrolysis of target polysaccharides. Enzymatic assays coupled with mass spectrometry analysis of digested oligosaccharide products provided further mechanistic insight into the hydrolase activity of the enzyme, which when incubated with Klebsiella, removes the capsule and sensitizes the cells to serum-induced killing. Overall, our findings expand our understanding of how phages target the Klebsiella capsule for infection, providing a further framework for the use of depolymerases as anti-virulence agents against this medically important pathogen.