The small Rho GTPase RAC1 is an essential regulator of cellular signaling that controls actin rearrangements and cell motility. Here， we identify a novel CUL3 RING ubiquitin ligase complex， containing the substrate adaptors KBTBD6 and KBTBD7， that mediates ubiquitylation and proteasomal degradation of TIAM1， a RAC1-specific GEF. Increasing the abundance of TIAM1 by depletion of KBTBD6 and/or KBTBD7 leads to elevated RAC1 activity， changes in actin morphology， loss of focal adhesions， reduced proliferation， and enhanced invasion. KBTBD6 and KBTBD7 employ ATG8 family-interacting motifs to bind preferentially to GABARAP proteins. Surprisingly， ubiquitylation and degradation of TIAM1 by CUL3(KBTBD6/KBTBD7) depends on its binding to GABARAP proteins. Our study reveals that recruitment of CUL3(KBTBD6/KBTBD7) to GABARAP-containing vesicles regulates the abundance of membrane-associated TIAM1 and subsequently spatially restricted RAC1 signaling. Besides their role in autophagy and trafficking， we uncovered a previously unknown function of GABARAP proteins as membrane-localized signaling scaffolds.