Development must be coordinated across body systems but must also accommodate cell-type-specific processes. We discovered that the gene regulatory circuit controlling developmental timing in the larval skin exhibits both points of convergence and divergence with the regulatory program governing the migration of the leader cell in gonad development, the distal tip cell (DTC). As a point of convergence, the conserved regulator of developmental timing, LIN-42/Period, peaks synchronously across cell types both during the L3 stage, when the DTC makes a turn in its normal migratory path, and the L4 stage in which the DTC normally continues straight ahead. We report that , like its ortholog , autorepresses its own transcription. is required cell-autonomously for proper pathfinding of the DTC; DTC-specific RNAi causes the DTC to turn in the mid-L4 instead of continuing straight ahead. We identified the FLYWCH transcription factor FLH-1 as able to directly bind the promoter. Using live-cell imaging, we show that double mutant DTCs have an aberrant turn in the mid-L4. These mutants derepress the L4 peak of expression in a stage- and DTC-specific manner, and this derepression is itself -dependent. During the aberrant mid-L4 turn in ; mutants, the focal adhesion factor TLN-1 is repolarized in the direction of turning. These results reveal that bodywide developmental rhythms can be fine-tuned to integrate with specific organogenic processes.