Bacterial cellulosic polymers constitute a prevalent class of biofilm matrix exopolysaccharides that rely on conserved cyclic diguanylate (c-di-GMP)-dependent cellulose synthases. Polymer structure and modifications, however, depend on the ensemble of synthase modules and accessory subunits, thus defining several types of bacterial cellulose secretion (Bcs) systems. InE. coli, a BcsRQABEFG macrocomplex, encompassing the inner membrane and cytosolic subunits, and an outer membrane porin, BcsC, secure the biogenesis of phosphoethanolamine (pEtN)-modified cellulose. Resolution-limited studies have proposed different macrocomplex stoichiometries and its assembly and regulation have remained elusive. Using cryo-EM, we visualize the molecular mechanisms of BcsA-dependent recruitment and stabilization of a trimeric BcsG pEtN-transferase for polymer modification and a dimeric BcsF-dependent recruitment of an otherwise cytosolic BcsE2R2Q2regulatory complex. We further demonstrate that BcsE, a secondary c-di-GMP sensor, remains dinucleotide-bound and retains the essential-for-secretion BcsRQ partners onto the synthase even in the absence of direct c-di-GMP-synthase complexation, likely lowering the threshold for c-di-GMP-dependent synthase activation. Such ‘activation-by-proxy’ mechanism could allow Bcs secretion system activation even in the absence of dramatic intracellular c-di-GMP increase and is reminiscent of other widespread synthase-dependent polysaccharide secretion systems where c-di-GMP sensing and/or synthase stabilization are carried out by key co-polymerase subunits.