Carbapenem-resistant Acinetobacter baumannii was recently named the top priority pathogen by the CDC, urgently requiring research and development of new antimicrobial strategies. It is responsible of frequent, hard-to-treat and often fatal healthcare-associated infections. Phage therapy, the use of viruses that infect and kill bacteria, is an approach gaining significant clinical interest. One major limitation for phage therapy is that bacteria can quickly develop resistance against phages, thus limiting their clinical potential. Here, we isolated phages from sewage samples and demonstrated their activity against a panel of A. baumannii strains. Two of the phages, targeting the clinical strains AB900 and carbapenem-resistant A9844 were characterized in detail. Co-incubation of the phages with their hosts in vitro resulted in the rapid emergence of phage-resistant bacterial mutants. Comparative bacterial genome analyses found the phage-resistant mutants harbored loss-of-function mutations in genes from the K locus, involved in the biosynthesis of A. baumannii’s capsule polysaccharides. Using genetic engineering, phage adsorption assays, and quantitative evaluation of capsule production, we demonstrated that the phages could not attach to the capsule-deficient mutants, establishing the bacterial capsule as the primary phage receptor in A. baumannii. As additional consequences of impaired capsule production, the phage-resistant strains could not form biofilms, became fully sensitized to the human complement system and alternative phages, and showed increased susceptibility to the antibiotics ampicillin/sulbactam, ceftazidime, imipenem, ciprofloxacin and minocycline. Finally, the phage-resistant isolates demonstrated a diminished capacity to colonize blood and solid tissues within a murine model of bacteremia. We demonstrate that phages can be used not only for their lytic activity but, if combined with a posteriori knowledge of their receptors and the mechanism of bacterial phage-resistance, for their potential synergy with other antimicrobial agents, opening the door to the next generation of phage therapy.