Flavobacteriia are recognized as key players in the marine carbon cycle, due to their ability to efficiently degrade algal polysaccharides both in the open ocean and in coastal regions. The chemical complexity of algal polysaccharides, their differences between algal groups and variations through time and space, imply that marine flavobacteria have evolved dedicated degradation mechanisms and regulation of their metabolism during interactions with algae. In the present study, we report the first transcriptome-wide gene expression analysis for an alga-associated flavobacterium during polysaccharide degradation. Zobellia galactanivorans Dsij(T), originally isolated from a red alga, was grown in minimal medium with either glucose (used as a reference monosaccharide) or one selected algal polysaccharide from brown (alginate, laminarin) or red algae (agar, porphyran, ι- or κ-carrageenan) as sole carbon source. Expression profiles were determined using whole-genome microarrays. Integration of genomic knowledge with the automatic building of a co-expression network allowed the experimental validation of operon-like transcription units. Differential expression analysis revealed large transcriptomic shifts depending on the carbon source. Unexpectedly, transcriptomes shared common signatures when growing on chemically divergent polysaccharides from the same algal phylum. Together with the induction of numerous transcription factors, this hints at complex regulation events that fine-tune the cell behavior during interactions with algal biomass in the marine environment. The results further highlight genes and loci that may participate in polysaccharide utilization, notably encoding Carbohydrate Active enZymes (CAZymes) and glycan binding proteins together with a number of proteins of unknown function. This constitutes a set of candidate genes potentially representing new substrate specificities. By providing an unprecedented view of global transcriptomic responses during polysaccharide utilization in an alga-associated model flavobacterium, this study expands the current knowledge on the functional role of flavobacteria in the marine carbon cycle and on their interactions with algae.