Parasites competing over limited host resources are faced with a tradeoff between reproductive success and host overexploitation jeopardizing survival. Surprisingly little is known about the outcome of such competitive scenarios, and we therefore aimed at elucidating interactions between the trematodes Himasthla elongata and Renicola roscovita coinfecting the periwinkle first intermediate host. The results show that the success of Himasthla colonies (rediae) in terms of cercarial emission is unaffected by Renicola competition (sporocysts), whereas deteriating host condition decreases fitness. Furthermore, double infection has no bearing on Himasthla’s colony size but elevated the proportion of non-reproductive rediae that play a decisive role in colony defence. Opposite, the development of the Renicola colony (size/maturity), and in turn fitness, is markedly reduced in presence of Himasthla, whereas the nutritional state of the host appears less important. Hence, the intramolluscan competition between Himasthla and Renicola is asymmetrical, Himasthla being the superior competitor. Himasthla not only adjusts its virulence according to the hosts immediate nutritional state, it also nullifies the negative impact of a heterospecific competitor on own fitness. The latter is argued to follow in part from direct predation on the competitor, for which purpose more defensive non-reproductive rediae are strategically produced.