The demosponge Crambe crambe shows a peculiar spermatogenesis, hard to be reconciled with the basal position of sponges in the animal phylogeny. Early spermatogenesis stages showed most of the simple features expected in sponges. However, spermiogenesis departed from the anticipated process. Spermatids lengthened remarkably, forming a deep cytoplasmic pit around the cilium insertion, with the proximal axoneme bending to produce a V-shaped spermatozoon surprisingly similar to that known in the phylum Phoronida. The cytology was unexpectedly complex, with a needle-like nucleus of helically condensed chromatin, a conical acrosome with a subacrosomal rod, and a mitochondrion connected to the basal body by striated rootlets. These findings establish that the spermatozoon of broad-casting demosponges occurs in two structural categories (‘primitive’ and ‘modified’ type). This dualistic condition must necessarily have pre-dated the evolutionary apparition of higher metazoans, if we are to keep regarding sponges as the most primitive animals. We hypothesize that internal fertilization in C. crambe– and incidentally other demosponges – may depart from the general model assumed for spermcasting sponges. The V-shape of this spermatozoon suggests a design to favour autonomous penetration through the dense mesohyl to reach the oocytes, rather than engulfment and transportation by carrier cells towards the oocyte. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 413–426.