Emiliania huxleyi is a bloom forming coccolithophore that impacts the global sulfur cycle by producing large amounts of dimethylsulfoniopropionate (DMSP) and its volatile metabolic product dimethyl sulfide (DMS). Top-down regulation of E. huxleyi blooms is attributed to viruses and grazers, however, the possible involvement of algicidal bacteria in bloom demise is underexplored. We isolated a Roseobacter strain, Sulfitobacter D7, from a North Atlantic E. huxleyi bloom. Co-culturing of Sulfitobacter D7 with E. huxleyi led to induction of algal cell death along with bacterial proliferation, exhibiting three defined phases of interaction. Sulfitobacter D7 consumed algae-derived DMSP and produced high amounts of methanethiol (MeSH), an alternative product of DMSP catabolism. Differential release of dissolved DMSP by E. huxleyi strains was highly correlated with Sulfitobacter D7 abundance and pathogenicity dynamics during co-culturing. Sulfitobacter D7 was highly prevalent during an oceanic E. huxleyi bloom and its abundance correlated with dissolved DMSP concentration. We propose that Roseobacters have an important role in E. huxleyi bloom demise mediated by metabolic requirement for algae-derived DMSP, thereby switching the fate of DMSP away from DMS towards MeSH. The balance between these competing DMSP catabolic pathways, driven by microbial interactions, may regulate oceanic sulfur cycling and feedback to the atmosphere.