Bacterial infections are a growing health concern worldwide and alternative treatment options are urgently needed to combat this new pandemic. Bacteriophages prey on their hosts irrespective of antibiotic-resistance and have been long recognised as an alternative means of combating infections. However, their unreliable performance in vivo despite their high in vitro potency has hindered their adoption as a reliable treatment option. Similarly, survival of drug-sensitive bacteria to antibiotic treatment has been linked to persistence of non-growing, dormant cells inside patients and evolution of antibiotic resistance. Given the high abundance of non-growing bacteria in the environment, we reasoned that some phages capable of infecting dormant, antibiotic-tolerant cells should exist. Through extensive screening of environmental samples, we isolated a new Pseudomonas aeruginosa phage which we named Paride. Paride can kill over 99% of cells in non-growing cultures harbouring high numbers of antibiotic-tolerant bacteria. Combined with the carbapenem meropenem, Paride led to the sterilization of these cultures, and this synergy was also observed in a murine model of a chronic P. aeruginosa implant infection. Furthermore, we show that efficient replication of Paride on dormant hosts depends on the same bacterial stress responses known to drive antibiotic tolerance. Therefore, we propose that Paride exploits vulnerabilities of the dormant physiology of antibiotic-tolerant bacteria and that understanding the underlying molecular mechanisms of these vulnerabilities will inspire novel therapeutic approaches to combat and prevent the emergence of treatment-resistant infections.