Within-host competition can affect outcomes of infections when parasites occupy the same niche. We investigated within-host competition and infection outcomes in Chinook salmon exposed to two genotypes of (myxozoan parasite). We assessed i) virulence (host mortality, median days to death), ii) within-host competition (abundance in host), and iii) success (spore production, proportion of myxospore-producing hosts) following concurrent and sequential exposures to single or mixed-genotype treatments. In single treatments, genotype-I replicated faster, and caused higher and earlier host mortality (higher virulence) but genotype-II produced more myxospores (higher success). In mixed treatments, costs of competition were observed for both genotypes evidenced by reduced replication or myxospore production following concurrent exposures, but only the less-virulent genotype suffered costs of competition when hosts were exposed to genotypes sequentially. To understand potential host effects on competition outcomes, we characterized systemic (spleen) and local (intestine) cytokine and immunoglobulin expression in single and mixed infections. We observed delayed systemic and immunosuppressive responses to the virulent genotype (I), rapid, localized and non-suppressive responses to the less-virulent genotype (II), and a combination of responses to mixed-genotypes. Thus, competition outcomes favoring the virulent genotype may be partially explained by the localized response to genotype-II that facilitates myxospore production (success) offsetting the systemic response to genotype-I that results in early inflammation and immunosuppression (that increases onset of mortality). This evidence for different but simultaneous responses to each genotype suggests selection should favor the exclusion of the weaker competitor and the evolution of increased virulence in the stronger competitor because the outcome was generally more costly for the less-virulent genotype. With caveats, our results are relevant for understanding infection outcomes in commercially and ecologically important salmonids in endemic regions where mixed infections are commonplace.