Spread of multidrug-resistant Pseudomonas aeruginosa strains threatens to render currently available antibiotics obsolete, with limited prospects for the development of new antibiotics. Lytic bacteriophages (phages), the natural predators of bacteria, represent a path to combat this threat. In vitro directed evolution is traditionally applied to expand the phage host range or increase bacterial suppression in planktonic cultures. However, while 80% of human microbial infections are biofilm-associated, research towards targeted improvement of phages’ ability to combat biofilms remains scarce. Here, we describe an in vitro evolution assay that improves multiple phage parameters in parallel, while optimizing phage cocktail design by exploiting a bacterial phage resistance trade-off. The obtained evolved phages show an expanded host spectrum, improved antimicrobial efficacy under isothermal microcalorimetric monitoring and enhanced antibiofilm performance, as determined by RT-qPCR. Our two-phage cocktail revealed further improved antimicrobial efficacy without incurring dual-phage-resistance in treated bacteria. We anticipate this assay will allow a better understanding of phenotypic-genomic relationships in phages and enable the training of phages against other desired pathogens. This, in turn, will strengthen phage therapy as a treatment adjunct to improve clinical outcomes of multidrug-resistant bacterial infections.