The morphology of gametangia was examined in 43 pairs of isolates (mating types A1×A2; 11 A1 and 24 A2 isolates; five isozyme/electrophoretic types) of Phytophthora cinnamomi. An amphigynous antheridium always formed with each oogonium. However, in 41 of the crosses a proportion (39 had 0·2–10% and two had >30%) of oogonia also consistently had single or multiple paragynous antheridia. Single or multiple paragynous antheridia formed concurrently with amphigynous ones during the period of gametangial production in paired colonies. Where there were multiple paragynous antheridia associated with an oogonium, sometimes additional antheridia formed after fertilization or even after oospores were visible. Developmental studies showed that when meiosis in amphigynous and paragynous antheridia was simultaneous, fertilization tubes developed synchronously from both. However, cytological examination indicated that either a nucleus from an amphigynous or a paragynous antheridium fertilized the oosphere. Observations of paragynous and amphigynous, and amphigynous-only associations suggested that fertilization from either type of antheridium only occurred when meiosis in the oogonium was nearly synchronous with that of the antheridium. Asynchronous meiosis between oogonia and antheridia may contribute to failed fertilization and aborted oospore development. This appears to be the first description of paragynous antheridia in P. cinnamomi and the second observation of oogonia with both paragynous and amphigynous antheridia in a heterothallic Phytophthora species. Moreover, the development of both paragynous and amphigynous antheridia with an oogonium is rare in Phytophthora, as is the development of multiple antheridia. Antheridial variation is a characteristic to be taken into account in isolate identification. Nuclei from paragynous antheridia appear able to fertilize oospheres and therefore, have a role in sexual reproduction.