The life cycle of the first known dinoflagellate parasite of stickleback is described in greater detail. The dinoflagellates are probably preglacial relicts that were introduced to the Queen Charlotte Islands on stickleback that have a common ancestry with a species from Japan, rather than North America. Important new discoveries include: lobose, rhizopodial and spheroid amoebae; a vegetative dinokaryon; the dinospore stage; an aplanozygote; bacterial symbionts throughout the life cycle; and amoeboid resting cysts containing modified chloroplasts. Although it is a fish parasite, this dinoflagellate bears closer affinity to the Phytodiniales than the Blastodiniales, because of the presence of amoeboid stages; a predominant autotrophic, active coccoid cyst; a transient trophont stage; and a variety of resting cysts. It has the uncharacteristic features of a temporary dinokaryon (dinokaryon in dinospore, vegetative and temporary cysts but eukaryon in amoebae and resting cysts) and palintomic sporogenesis, both of which were previously reserved for the Blastodiniales. This raises important questions about the classification of parasitic dinoflagellates in general and underscores the need for re-examination of these taxa.