Abstract Dinoflagellates are a diverse group of phytoplankton, ranging from harmful bloom-forming microalgae to photosymbionts of coral reefs. Genome-scale data from dinoflagellates reveal atypical genomic features, extensive genomic divergence, and lineage-specific innovation of gene functions. Long non-coding RNAs (lncRNAs), known to regulate gene expression in eukaryotes, are largely unexplored in dinoflagellates. Here, using high-quality genome and transcriptome data, we identified 48039 polyadenylated lncRNAs in three dinoflagellate species: the coral symbionts Cladocopium proliferum and Durusdinium trenchii, and the bloom-forming species, Prorocentrum cordatum. These lncRNAs have fewer introns and lower G+C content than protein-coding sequences; 37 768 (78.6%) are unique with respect to sequence similarity. We classified all lncRNAs based on conserved motifs (k-mers) into distinct clusters, following properties of protein-binding and/or subcellular localisation. Interestingly, 3708 (7.7%) lncRNAs are differentially expressed under heat stress, algal lifestyle, and/or growth phase, and share co-expression patterns with protein-coding genes. Based on inferred triplex interactions between lncRNA and putative promoter regions, we identified 19 460 putative gene targets for 3721 lncRNAs; 907 genes exhibit differential expression under heat stress. These results reveal, for the first time, the diversity of lncRNAs in dinoflagellates and how lncRNAs may regulate gene expression as a heat-stress response in these ecologically important microbes.