Harmful algal blooms (HABs) or “red tides” are some of the most reported incidents caused by warming oceans, contributing to losses of USD 7.5B per year in fisheries and aquaculture worldwide. Specifically, over-abundance of blooming dinoflagellate microalgae results in imbalanced cycling of nitrogen and carbon, and accumulation of toxins that are lethal to other organisms in high doses. However, the molecular and evolutionary mechanisms that underpin the capacity of these dinoflagellates to bloom remain little known. Here, we present the first sequenced genome of a bloom-forming “red tide” dinoflagellate, Prorocentrum cordatum, and the transcriptome, proteome, and metabolome data from axenic cell cultures to elucidate their molecular responses to heat stress. Compared to other available dinoflagellate genomes, genome of P. cordatum (4.75 Gb) exhibits the highest G+C (mean 59.7%) and the longest introns (mean 4.7 Kb), with high repeat content (61% of genome bases) and extensively duplicated gene functions that are essential for metabolism, cell signalling and stress response. We found concerted molecular responses that are general to heat stress, or specific to the level of severity, implicating functions for energy production e.g. photosynthesis, and energy consumption e.g. protein synthesis. We also identified differential editing of mRNAs and usage of exons that regulate expression of genes, some are individual genes that each encodes multiple full-length proteins. Our results demonstrate the genomic hallmark of a free-living, bloom-forming dinoflagellate, and how complex genome and gene structures in combination with multi-level transcriptional regulations contribute to the resilience of P. cordatum in warming environments. Data and knowledge generated from this work provide a useful reference for research in dinoflagellates and other marine microbial eukaryotes, and novel insights into the ecology and evolution of bloomability in microalgae.