The Pacific sector of the Arctic Ocean, a region with the fastest sea-ice loss in recent decades, is experiencing unprecedented biological regime shifts in its marine ecosystems today. However, a shelf-wide characterization of marine plankton communities over this region and environmental processes behind it remain largely unresolved, despite phytoplankton phenology is now considered to be an important factor for assessing how Arctic Ocean interacts with global climate change. Here, we present the first detailed description of recent dinoflagellate cyst assemblages in 32 surface sediment samples from the Chukchi–East Siberian Sea shelves, the Pacific Arctic Ocean, to examine their biogeographic patterns and associated environmental forcing factors. We find a strong regionalization in the species composition and distribution along the shallow-shelf cyst accumulation zone; in the Chukchi Sea sector, northward flow of warm-Pacific water along with extreme seasonality, sufficient nutrient supplies and higher light availability leads to a large occupation of cosmopolitan, opportunistic-nature taxa, whilst the East Siberian Sea sector with more extensive sea-ice cover and lower temperatures is primarily dominated by “round brown spiny cyst” taxa that have a strong affinity for cold, polar conditions. Specifically, an exclusive dominance of heterotrophic taxa at the East Siberian Sea region is inferred to be closely tied to Atlantic-origin water intrusions that lift nutrient-rich, cold bottom water up to oligotrophic surface layer to grow diatoms and other prey organisms. The observed contrast in this geographical “hot spot”, where the Pacific- and Atlantic-origin waters face each other, clearly manifests a growing expansion of southern waters into an increasingly ice-free Arctic Ocean that reshapes Arctic Ocean biogeography from the base of marine food chains. Our study highlights considerable potential of dinoflagellate cysts as a valuable environmental proxy to indicate complex interactions between ocean physics and marine biology under the rapidly changing Arctic climate system.