Harmful algal blooms (HABs) of the toxic haptophyte Prymnesium parvum are a recurrent problem around the world. Strains of P. parvum vary in the toxins they produce and in other physiological traits associated with HABs, but the genetic basis for this variation is unknown. To investigate genome diversity in this morphospecies, we generated genome assemblies for fifteen diverse strains of P. parvum. Comparative analysis revealed considerable DNA content variation between strains. Strains included haploids, diploids, and polyploids, but not all differences in DNA content were due to variation in genome copy number. Haploid genome size between strains of different chemotypes differed by as much as 243 Mbp. Syntenic and phylogenetic analyses indicate that the Texas strain UTEX 2797 is a hybrid that retains two phylogenetically distinct haplotypes. Investigation of gene families variably present across strains identified functional categories associated with metabolic and genome size variation in P. parvum including genes for biosynthesis of toxic metabolites and proliferation of transposable elements. Together, our results indicate that P. parvum is comprised of multiple cryptic species. Using these genome resources, we identified giant polyketide synthase enzymes (PKZILLAs) for prymnesin toxin biosynthesis and characterized variation at the PKZILLA loci responsible for differences in prymnesin structure. These genomes provide a robust phylogenetic and genomic framework for investigations into the eco-physiological consequences of the intra- and inter-specific genetic variation present in P. parvum blooms and demonstrate the need for similar resources for other HAB-forming morphospecies.