Spire-bearing brachiopods formally comprise four different rhynchonelliform orders. A calcified spiral brachidium (presumably supporting a spirolophe when alive) and variable median fold and sulcus (probably aiding separation of incurrent from excurrent flows) are peculiar characteristics they all share. Inferences regarding feeding current systems for these extinct taxa have long remained controversial. Two rival models (the Williams–Ager model and the Rudwick–Vogel model) have been developed, each of which has gained supporters as well as critics over the years. In this present paper they are both contrasted and reassessed on the basis of available evidence, together with a new approach that combines: (a) a morpho-functional analysis applying the plankton net as a suitable seston-collecting paradigm; (b) a review of actualistic data showing that all extant spirolophes are functionally inhalant (irrespective of water entering the valves laterally or not); (c) an evaluation of known outcomes from flume experiments yielding consistent empirical results where gaping shells are oriented transversally and dorsally upcurrent; and (d) a reappraisal of the distributions of certain epizoobionts and endosymbionts revealing compatible patterns. The evidence thus accumulated supports the main conclusion that, in most groups (with laterally tapering spiralia), the inhalant current was located medially with the exhalant currents on either side; only in atrypides (with centrally to dorsally tapering spiralia) does the reverse situation appear to have occurred.