Cyanobacteria are photoautotrophs that profoundly impact the biogeochemical cycles on Earth. Due to their photosynthetic lifestyle that includes the fixation of atmospheric CO2, they are of increasing interest for a sustainable economy. Knowledge of protein expression and regulation is key for understanding of the cyanobacterial metabolism; however, proteome studies in cyanobacteria are still limited and cover only a fraction of the theoretical proteome. Here, we performed a proteogenomic analysis of 628 LC-MS/MS measurements for the unicellular model cyanobacterium Synechocystis sp. PCC 6803 to characterize the expressed (phospho)proteome, re-annotate known and discover potential novel open reading frames (ORFs). By mapping extensive shotgun MS proteomics data generated by the SCyCode consortium onto a six-frame translation of the Synechocystis genome, we re-annotated 96 start sites and discovered 103 novel open reading frames (ORFs). Through re-analysis of previously published multi-omics datasets, we confirmed 48 re-annotated or novel ORFs with high confidence. Our study resulted in the largest reported proteome and phosphoproteome dataset for Synechocystis, covering expression of about 80% of the theoretical proteome and 642 O-phosphorylation events under various cultivation conditions, such as nitrogen or carbon limitation. This dataset will serve as a resource providing dedicated information on condition-dependent protein expression and phosphorylation.