Background Carbapenem-non-susceptible Pseudomonas aeruginosa (CnSPA) bloodstream infections (BSIs) are associated with high mortality and limited treatment options, yet long-term genomic-clinical data from China are scarce. Methods We retrospectively analyzed 52 non-duplicate CnSPA isolates causing BSIs from 2014 to 2023 in a tertiary hospital in eastern China. Whole-genome sequencing was used to characterize antimicrobial resistance genes (ARGs), carbapenem resistance-associated mutations, mobile genetic elements, sequence types (STs), serotypes, genetic relationship, and integron structures. Clinical data were integrated to identify risk factors for mortality and polymicrobial BSIs. Results CnSPA isolates showed high resistance to imipenem (98.1%) and multiple beta-lactams and fluoroquinolones, while remaining susceptible to colistin. Carbapenemase genes were rare, whereas diverse ARGs, frequent oprD and ampC mutations, and widespread co-localization of ARGs with insertion sequences supported a major role for non-carbapenemase mechanisms and mobile genetic elements in resistance dissemination. Thirty-six distinct STs-including high-risk clones ST235, ST244, ST274, and ST357, heterogeneous serotypes and phylogenetic tree indicated substantial genomic diversity. Integron analysis revealed structurally diverse complete integrons, CALINs, and In0 elements in a subset of genomes. Clinically, mortality was 38.5%; prior carbapenem exposure, organ failure, and prolonged mechanical ventilation were independent predictors of death, while long-term catheterization was associated with polymicrobial BSIs. Conclusions CnSPA BSIs in this setting are driven by multifactorial resistance mechanisms, high-risk clones, and mobile genetic elements, with modifiable clinical factors strongly linked to poor outcomes.