Haptoglossa dickii is a biflagellate zoosporic parasite of bactivorous nematodes. The walled encysted zoospores germinate more or less synchronously to produce specialised infection cells known as gun cells. This paper documents the changes in the main cytoplasmic organelles, namely the nucleus, Golgi body, mitochondria, lipid droplets and dense-body vesicles, from the onset of encystment until the formation of the mature gun cell. The septum-delimited gun cells show a marked polarity in the distribution of their organelles from their inception, which seems in part determined by the temporal order by which the main organelles migrate out of the cyst and into the gun cell initial. In this species the majority of dense-body vesicles and mitochondria precede the nucleus and lipid droplets. The nucleus remains more or less central throughout the remaining course of gun cell differentiation. The single nucleus associated Golgi body changes its orientation to track (possibly even determining) the spatial position of the ingrowing injection tube. The mitochondria fuse to form one or more complex reticulate structures which are aligned close to the injection tube throughout its formation and which in the mature cells form a fine network entwined around the fully differentiated tube. The vesicles containing electron-dense inclusion granules (dense-body vesicles) are initially concentrated towards the gun cell anterior, but later migrate to the posterior end of the cell and fuse to give rise to the basal vacuole. Some of the likely functional aspects of these cytoplasmic changes are discussed.