Proteins commonly fold co-translationally at the ribosome, while the nascent chain emerges from the ribosomal exit tunnel. Protein domains that are sufficiently small can even fold while still located inside the tunnel. However, the effect of the tunnel on the folding dynamics of these domains is not well understood. Here, we combine optical tweezers with single-molecule FRET and molecular dynamics simulations to investigate folding of the small zinc-finger domain ADR1a inside and at the vestibule of the ribosomal tunnel. The tunnel is found to accelerate folding and stabilize the folded state, reminiscent of the effects of chaperonins. However, a simple mechanism involving stabilization by confinement does not explain the results. Instead, it appears that electrostatic interactions between the protein and ribosome contribute to the observed folding acceleration and stabilization of ADR1a. Wruck et al. investigate the folding of the small zinc-finger domain ADR1a inside and at the vestibule of the ribosomal tunnel, using optical tweezers, single-molecule FRET, and molecular dynamics simulations. They find that the ribosomal tunnel accelerates folding while stabilizing the folded state like chaperonins. This study provides insights into the role of the ribosomal tunnel in the folding dynamics of nascent polypeptides.