We have characterized the responses of the opportunistic pathogen Pseudomonas aeruginosa to prolonged starvation for carbon or nitrogen sources, and to transitions between these states. We find that most cells survive both types of starvation for more than a week and maintain low but robustly detectable levels of protein synthesis in the absence of growth. Nitrogen-starved cells are larger, make more proteins and retain fewer ribosomes than carbon-starved cells, indicating that distinct physiological strategies are adopted during the two starvation types. We found that the total proteomes collected from starved cells at different times during a starvation transition were not very different from each other but were distinct from those of growing cells. By combining this dataset with a nascent (BONCAT) proteomics dataset and a transposon insertion sequencing (TnSeq) dataset, we highlight proteases and chaperones; flagellar motility; and the nitrogen-related phosphotransferase system as key fitness-impacting functions that are actively maintained by growth arrested Pseudomonas aeruginosa.