The picocyanobacterium Synechococcus is a prominent primary producer in the marine environment. The marine Synechococcus strains are clustered into different clades representing ecologically distinct genotypes. In this study, we compared phylogeny, photophysiology and cell cycles of four novel phycoerythrin-containing Synechococcus strains (clade II of subcluster 5.1) isolated from different depths of the water column (surface and subsurface waters) in coastal and offshore regions of the eastern Arabian Sea. The surface water strains possessed a lesser number of thylakoid layers and had a higher zeaxanthin to chlorophyll a ratio than subsurface strains indicating possible influence of light intensity available at their niche. The DNA distribution pattern of the four strains was bimodal in optimal cellular physiology conditions with cell division restricted to the light period and synchronized with the light–dark cycle. The presence of phycourobilin or phycoerythrobilin and the ratio between these two chromophores in all four strains varied according to available spectral wavelength in situ. This study indicates that the timing of cell division is conserved within these genotypically identical Synechococcus strains, despite their having different chromophore ratios. We conclude that the timing of cell division of the Synechococcus strains has a genetic basis rather than being determined by phenotypic characters, such as chromophore content and ratio.