Throughout eukaryotes, the synaptonemal complex (SC) is a supramolecular structure essential for meiotic chromosome dynamics and sexual reproduction. While metazoan SC proteins display substantial sequence divergence, the lack of functional analyses beyond bilaterian models has obscured a mechanistic understanding of SC evolution. Here, we report that the sea anemone Nematostella vectensis exhibits synapsis of homologous chromosomes in a classic zipper-like manner and expresses at least eight orthologs of 10 known vertebrate SC proteins. Unexpectedly, mutagenesis of the core SC components sycp1, syce2, and sycp3 resulted in divergent and sexually dimorphic phenotypes, indicating the functional diversification of these conserved factors. Combined, these findings challenge the assumption that the conservation of protein sequence or ultrastructure implies mechanistic homology.