Lytic phages hydrolyze the host cell wall at the end of their reproductive cycle to induce lysis and release of their progeny. To do this, they produce endolysins, which hydrolyze the cell wall, and holins, which allow the endolysins access to the cell wall. The mechanism by which the holins permeabilize the cytoplasmic membrane is not clear. However, it is currently assumed, primarily based on studies on phage T4 and lambda systems, that holins form two-dimensional aggregates (rafts) that dissolve large areas of the cytoplasmic membrane at the required time point. Using the phage T4 system as model, we now show that smaller assemblies are sufficient to enable the release of endolysin into the periplasm and that positions of the cytoplasmic domain of the holin and therein especially in the N-terminal amphipathic helix are essential for this. AlphaFold 3 predicts a reasonable ring structure for T4 holin, which is consistent with our data, as the important amphipathic helix generates a hydrophilic hole that could enable a passage of the endolysin. Ring formation and a thereby induced flipping of the amphipathic helix might be a general mechanism for hole formation by holins, which would clarify an old key question of phage cycle biology.