Cilia and flagella are dynamic organelles that undergo assembly and disassembly during each cell cycle. They are structurally polarized, and the mechanisms by which these organelles are disassembled are incompletely understood. Here, we show that flagellar resorption occurs in two distinct phases of length-dependent regulation. A CDK-like kinase, encoded by flagellar shortening 1 (FLS1), is required for the normal rate of disassembly of only the distal part of the flagellum. Mechanistically, loss of function of FLS1 prevents the initial phosphorylation of CALK, an aurora-like kinase that regulates flagellar shortening, and induces the earlier onset of the inhibitory phosphorylation of CrKinesin13, a microtubule depolymerase, which is involved in flagellar shortening. In addition, CALK and CrKinesin13 phosphorylation can also be induced by the process of flagellar shortening itself, demonstrating an example of cilia-generated signaling not requiring the binding of a ligand or the stimulation of an ion channel.