Many of the diverse functions of cilia depend upon tight control of their length. Steady-state length reflects a balance between rates of ciliary assembly and disassembly, two parameters likely controlled by a length sensor of unknown identity or mechanism. A null mutation in Chlamydomonas CNK2, a member of the evolutionarily conserved family of NIMA-related kinases, reveals feedback regulation of assembly and disassembly rates. cnk2-1 mutant cells have a mild long-flagella (lf) phenotype as a consequence of reduced rates of flagellar disassembly. This is in contrast to the strong lf mutant lf4-7, which exhibits an aberrantly high rate of assembly. Cells carrying both mutations have even longer flagella than lf4-7 single mutants do. In addition to their high rate of assembly, lf4-7 mutants have a CNK2-dependent increase in disassembly rate. Finally, cnk2-1 cells have a decreased rate of turnover of flagellar subunits at the tip of the flagellum, demonstrating that the effects on disassembly are compensated by a reduced rate of assembly. We propose a model wherein CNK2 and LF4 modulate rates of disassembly and assembly respectively in a feedback loop that is activated when flagella exceed optimal length. •Chlamydomonas cells null for the CNK2 kinase have a mild long-flagella phenotype•cnk2-1 cells are defective in flagellar disassembly and therefore resorption•The cnk2-1 mutation enhances the long-flagella phenotype of lf4-7 mutants•cnk2-1 cells exhibit a compensatory decrease in incorporation of new tubulin