Dinoflagellates are a large, ecologically important phylum of marine unicellular algae. Their huge genomes make it highly challenging to decipher the genetic basis of key processes such as harmful algal bloom (HAB) formation and response to warming oceans. To address these issues, we generated a high quality genome assembly from Prorocentrum cordatum, a globally abundant, HAB forming dinoflagellate. Our analyses demonstrate massive expansion of the gene inventory to 85,849 predicted genes, primarily driven by unusually long and frequent introns and dispersed duplicates enriched for bloom relevant functions. We find that cell yield is reduced at higher culture temperatures. To understand this response, we integrated transcriptome, proteome and metabolome data and identified both a global and a temperature specific heat-stress response. The underlying metabolic changes reflect damage to photosynthesis and central metabolism. The transcriptome data show that 25% of genes are differentially expressed under heat stress, with concomittant extensive RNA editing and alternative exon usage. Multi-codon genes and transcripts for HSP70 and RuBisCo suggest a polycistronic gene organisation. Our work represents the first genome based analysis of a red tide dinoflagellate and demonstrates that temperature resilience in P. cordatum is mediated by a unique genome structure and multi-level transcriptional regulation.