Dinoflagellates are key players in marine ecosystems, yet genomic underpinning of their unique cytology and exceptional ecological success is poorly understood. We present here the genome sequence of the reef coral endosymbiont Symbiodinium kawagutii. Illumina sequencing yielded 43.6 Gbp high-quality sequence, predicting a 1.18 Gbp genome size with 36,850 genes including 2,260 S. kawagutii-specific gene families. Surprisingly for dinoflagellates, the S. kawagutii genome is low in repetitive/duplicated regions and gene tandem arrays but rich in introns, features typical of other eukaryotes. We find that integrase, reverse transcriptase, transposases, and other genes apparently acquired via horizontal transfer are highly represented in the genome indicating the potential of active genome expansion. We found exceptionally high copy numbers of genes that are potentially responsible for the permanent condensation of chromosomes characteristic of the phylum. A high number of methylation-related genes were identified, consistent with the extensive DNA methylation in dinoflagellates. The genome harbors a wealth of epigenetic regulatory elements such as microRNA and histone modifying genes. We identified the complete machinery of splicing, apparently shared between cis and trans-splicing and mRNA editing. We also identified a suite of genes potentially associated with endosymbiosis and with response to stress. We have also assembled the first complete dinoflagellate pathways of tricarboxylic acid cycle, nutrient uptake and assimilation, and cell cycle regulation. This study provides a glimpse into the perplexing genome of a distinct group of eukaryotes and a basis on which to eventually decipher the numerous mysteries in this lineage.