Dinoflagellates, a class of unicellular eukaryotic phytoplankton, exhibit minimal transcriptional regulation, representing a unique model for exploring gene expression. The biosynthesis, distribution, regulation, and function of mRNA N1-methyladenosine (m(1)A) remain controversial due to its limited presence in typical eukaryotic mRNA. This study provides a comprehensive map of m(1)A in dinoflagellate mRNA and shows that m(1)A, rather than N6-methyladenosine (m(6)A), is the most prevalent internal mRNA modification in various dinoflagellate species, with an asymmetric distribution along mature transcripts. In Amphidinium carterae, we identify 6549 m(1)A sites characterized by a non-tRNA T-loop-like sequence motif within the transcripts of 3196 genes, many of which are involved in regulating carbon and nitrogen metabolism. Enriched within 3'UTRs, dinoflagellate mRNA m(1)A levels negatively correlate with translation efficiency. Nitrogen depletion further decreases mRNA m(1)A levels. Our data suggest that distinctive patterns of m(1)A modification might influence the expression of metabolism-related genes through translational control.