The comprehensive description of unicellular heterotrophic protists is essential for understanding the functioning of marine ecosystems and defining evolutionary relationships within marine microbial communities. For that reason, new insights into the functional genes of key protists, such as ciliates and dinoflagellates, are needed to complement the increasing taxonomic complexity and bridge the gap between various eco-functional processes in the ocean. In this study, single-cell transcriptomic sequencing proved to be an efficient method to create a snapshot of expressed genes of unicellular heterotrophs. We sequenced 65 single-cell transcriptomes from 20 fresh field samples collected from Sub-Arctic and North Sea waters. These 13 ciliate and 52 dinoflagellate transcriptomes will generally contribute to a greater understanding of functional and evolutionary processes of these marine protists. Further, we generated multi-gene phylogenies of several dozen genes to unravel the relationships of these heterotrophic taxa to other dinoflagellates and ciliates, respectively. These approaches also helped to elucidate the evolution of functional genes and traits for these understudied essential groups. Additionally, the datasets were incorporated into our metatranscriptomic reference database to fill the gap (of approx. 50%) of genomic information of heterotrophic organisms and their functional processes. Overall, identifying the phylogenetic relationships and functional diversity of heterotrophic and mixotrophic protists will clarify paramount marine microbial food web processes and provide clues to the system's sensitivity to climate change.