Phytoplankton blooms characterize temperate ocean margin zones in spring and contribute substantially to their high productivity. We investigated the bacterioplankton response to a diatom bloom in the North Sea and observed an as yet unseen dynamic succession of thriving populations at genus level resolution. Taxonomically distinct expressions of carbohydrate-active enzymes, transporters (in particular TonB-dependent transporters) and phosphate acquisition systems were found, indicating that distinct populations of Bacteroidetes, Gammaproteobacteria and Alphaproteobacteria acted like guilds specialized for successive algal-derived organic matter decomposition. Our results suggest that algal substrate availability and bacterial ecological niches determined the succession. A better understanding of such couplings between bacterioplankton and phytoplankton is needed to pave the way for predictive models of bacterioplankton bloom dynamics and thus more accurate global carbon turnover balances.