Cyanobacteria are important phytoplankton in the Baltic Sea, an estuarine-like environment with pronounced north to south gradients in salinity and nutrient concentrations. Here, we present a metagenomic and -transcriptomic survey, with subsequent analyses targeting the genetic identity, phylogenetic diversity, and spatial distribution of Baltic Sea cyanobacteria. The cyanobacterial community constituted close to 12% of the microbial population sampled during a pre-bloom period (June–July 2009). The community was dominated by unicellular picocyanobacteria, specifically a few highly abundant taxa (Synechococcus and Cyanobium) with a long tail of low abundance representatives, and local peaks of bloom-forming heterocystous taxa. Cyanobacteria in the Baltic Sea differed genetically from those in adjacent limnic and marine waters as well as from cultivated and sequenced picocyanobacterial strains. Diversity peaked at brackish salinities 3.5–16 psu, with low N:P ratios. A shift in community composition from brackish to marine strains was accompanied by a change in the repertoire and expression of genes involved in salt acclimation. Overall, the pre-bloom cyanobacterial population was more genetically diverse, widespread and abundant than previously documented, with unicellular picocyanobacteria being the most abundant clade along the entire Baltic Sea salinity gradient.