When Chlamydomonas cells resorb their flagella, seven polypeptides become asymmetrically dimethylated (aDMA) on arginine residues. Tandem mass spectrometry has identified these as radial spoke proteins 1, 2, 5, and 6; tektin, a structural component of the outer doublets; and flagellar-associated protein 172 (FAP172) (coiled-coil domain containing protein 40 (CCDC40)) and FAP250 (CCDC65), which are associated with inner arm dynein and the nexin-dynein regulatory complex. The enzyme protein arginine methyl transferase 1 (PRMT1), which generates aDMA residues, is a component of the flagellar matrix; antibodies to PRMT1 label full-length flagella in a punctate pattern along the length of the axoneme. During resorption, PRMT1 localization becomes enhanced at the flagellar tip, which is the site of the net disassembly of the flagellar axoneme, and gel shift assays indicate PRMT1 is phosphorylated under resorbing conditions. These data are consistent with a model in which a resorption signal activates one or more protein kinases, resulting in the up-regulation of the components of a protein methylation pathway resident in flagella. Methylation results in axonemal instability and/or enhances the interaction of axonemal polypeptides with intraflagellar transport particles, which then move disassembled components to the cell body for degradation or recycling.