Cilia of higher animals sense various environmental stimuli. Proper ciliary signaling requires appropriate extent of BBSome‐mediated export of membrane receptors across ciliary barrier transition zone (TZ) through retrograde intraflagellar transport (IFT) machinery. How the barrier passage is controlled, however, remains unknown. Here, we show that small GTPase Rabl2 functions as a molecular switch for the outward TZ passage. Rabl2‐GTP enters cilia by binding to IFT‐B complex. Its GTP hydrolysis enables the outward TZ passage of the BBSome and its cargos with retrograde IFT machinery, whereas its persistent association leads to their shedding from IFT‐B during the passing process and consequently ciliary retention. Rabl2 deficiency or expression of a GTP‐locked mutant impairs the ciliary hedgehog signaling without interfering with ciliation and respectively results in different spectrums of mouse developmental disorders. We propose that the switch role of Rabl2 ensures proper turnover of the BBSome and ciliary membrane receptors to fine‐tune cilia‐dependent signaling for normal embryonic development and organismic homeostasis. Synopsis: Cilliary signaling is adjusted via retention or export of ciliary receptors through the ciliary transition zone. The small GTPase Rabl2 fine‐tunes this process by GTP hydrolysis‐dependent gating of BBSome‐mediated membrane receptor export. Murine Rabl2 is dispensable for ciliogenesis and the ciliary entry of the IFT‐B ciliary transport complex.Rabl2‐GTP enters cilia by binding to IFT‐B.Ciliary Rabl2‐GTP impairs the exit of the BBSome complex and its cargos across the transition zone.Mice deficient in Rabl2 or expressing an active mutant show distinct developmental defects. [ABSTRACT FROM AUTHOR]