We describe new insights into the morphology and life history of the bizarre parasite Haplozoon axiothellae (Dinoflagellata) using light microscopy (LM), scanning electron microscopy (SEM), and confocal laser scanning microscopy (CLSM). Trophonts were isolated from the intestines of host maldanid polychaetes, Axiothella rubrocincta, collected from San Juan Island, Washington, USA. LM and SEM confirmed features previously observed, such as amphiesmal projections, mature and immature junctions between the nucleated compartments of the vermiform syncytium and visible polygonal alveoli. CLSM of adult trophonts fluorescently stained for DNA, tubulin, centrin, and plasma membrane demonstrated several new ultrastructural traits: (1) an extensive basket of parallel microtubules within the trophomere used for host attachment, (2) two physically separated MTOCs (i.e. putative pairs of basal bodies) beneath pores on the ventral side of each compartment, (3) robust mitotic and/or meiotic spindles associated with one to four nuclei in each compartment, (4) spindles with polar bodies that are disconnected from the MTOCs, (5) a centrin-stained fibril within the trophomeres that potentially functions to retract the motile stylet, and (6) cytokinesis in the posterior-most compartments. This study renames haplozoan compartments using the suffix “-mere” rather than “-cyte” (i.e. trophomere, gonomere, sporomere) to reflect their status within a single syncytium.