Dinoflagellates possess many unique cellular characteristics with unresolved evolutionary histories including nuclei with greatly expanded genomes and chromatin packaged using histone-like proteins and dinoflagellate-viral nucleoproteins instead of histones, highly reduced mitochondrial genomes with extensive RNA editing, a mix of photosynthetic and cryptic secondary plastids, and tertiary plastids. Resolving the evolutionary origin of these traits requires understanding their ancestral states and early intermediates. Several deep-branching dinoflagellate lineages are good candidates for such reconstruction, however they tend to be delicate and environmentally sparse, so such analyses are not always simple. Here, we employ transcriptome sequencing from manually-isolated and microscopically documented cells to resolve the placement of two cells of one such genus, Abedinium, collected by ROV in deep waters off the coast of Monterey Bay. One cell corresponds to the only described species, A. dasypus, while the second cell is distinct and formally described as Abedinium folium, sp. nov. Abedinium has classically been assigned to the deep-branching dinoflagellates subgroup Noctilucea, which is weakly supported by phylogenetic analyses of the single characterized gene from any member of the genus, small subunit ribosomal RNA (SSU rRNA). However, a phylogenetic analysis based on 221 proteins from the transcriptome places Abedinium in a distinct lineage, separate from and basal to the Noctilucea and the rest of the core dinoflagellates. The transcriptome also contains evidence of a cryptic plastid functioning in the biosynthesis of isoprenoids, iron-sulfur clusters, and heme, a mitochondrial genome with all three expected protein-coding genes (cob, cox1, and cox3), and the presence of some but not all dinoflagellate-specific chromatin packaging proteins.