Seasonal cycles of marine microbial communities are central to ocean carbon cycling. While bacterioplankton seasonality is well-defined, the in situ functional temporal dynamics of oceanic fungi (mycoplankton) remain unresolved. Existing insights come either from spatial omic surveys, which lack temporal resolution, or from temporal amplicon studies, which lack functional insight. Here, using a two-year metagenomic and metatranscriptomic time-series, we show that fungal enzymatic repertoires organic matter degradation undergo pronounced, rhythmic seasonal restructuring, tightly coupled to particle-associated niches. Although Ascomycota and Basidiomycota dominated year-round saprotrophy, early-diverging lineages (Mucoromycota and Chytridiomycota) surged in autumn and winter, revealing a dual strategy of saprotrophic degradation and parasitic potential. Enzyme expression tracked substrate availability, shifting from labile algal polysaccharides to resistant polymers and protein-rich detritus in autumn and winter. This functional reprogramming was orchestrated by temperature, salinity, phosphorus, and microbial community dynamics, highlighting the combined influence of environmental filtering and biotic interactions on fungal ecosystem functioning. Collectively, our findings establish mycoplankton as predictable, seasonally adaptive regulators of organic matter transformation and remineralization, underscoring the need to explicitly incorporate fungal succession into coastal biogeochemical models.