Dinoflagellates are major primary producers in the world’s oceans, the cause of harmful algal blooms, and endosymbionts of marine invertebrates. Much remains to be understood about their biology including their peculiar crystalline chromosomes. Here we used Hi-C to order short read-based sub-scaffolds into 94 chromosome-scale scaffolds of the genome of the coral endosymbiont Symbiodinium microadriaticum. Hi-C data show that chromosomes are folded as linear rods within which loci separated by up to several Mb are highly packed. Each chromosome is composed of a series of structural domains separated by boundaries. Genes are enriched towards the ends of chromosomes and are arranged in unidirectional blocks that alternate between top and bottom strands. Strikingly, the boundaries of chromosomal domains are positioned at sites where transcription of two gene blocks converges, indicating a correlation between gene orientation, transcription and chromosome folding. Some chromosomes are enriched for genes involved in specific biological processes (e.g., photosynthesis, and nitrogen-cycling), and functionally related genes tend to co-occur at adjacent sites in the genome. All chromosomes contain several repeated segments that are enriched in mobile elements. The assembly of the S. microadriaticum genome and initial description of its genetic and spatial organization provide a foundation for deeper exploration of the extraordinary biology of dinoflagellates and their chromosomes.