The foraging behaviour of Armillaria rhizomorph systems is poorly understood owing to their cryptic position within the soil. We investigated foraging in a homogeneous environment (i.e. agar), finding that rhizomorph systems of the more parasitic species, A. mellea, A. ostoyae, and A. tabescens, lacked melanin and the approximately cylindrical cord-like form observed in the field. In contrast, rhizomorph systems of the more saprotrophic species, A. calvescens, A. gallica, and A. sinapina, developed radially resembling those in the field. For the three saprotrophic Armillaria species, the number of rhizomorph tips, total rhizomorph length and total rhizomorph surface area were significantly positively correlated with increasing rhizomorph system diameter and elapsed time in two developmental tests. However, the fractal dimension (D), used as a measure of foraging intensity, was temporally invariable, suggesting that one component of foraging behaviour is innate. In a heterogeneous environment (i.e. sand) and in the absence of a potential nutrient source, we observed that rhizomorph systems of A. gallica most often developed asymmetrically. While rhizomorph foraging was unresponsive to the lateral placement of an uncolonised stem segment, we were able to demonstrate directional growth toward an uncolonised Quercus velutina stem segment placed above or below the colonised source stem segment. When neighboring rhizomorph systems were conspecific genets of A. gallica, we observed that the growth of one rhizomorph system was directed toward zones unoccupied by its neighbour. However, the foraging intensity of the neighbouring genets, as measured by fractal dimension (D), was unaffected by the proximity of a neighbour. When neighbouring rhizomorph systems represented different species (A. gallica and A. mellea), A. gallica rhizomorph systems produced more total length and more foraging tips but concentrated their rhizomorph production away from the neighbouring A. mellea genet. In contrast, A. mellea rhizomorph systems produced significantly more foraging tips per unit length, both overall and in the zone of confrontation with the neighbouring A. gallica genet. Our observations are consistent with field observations of territoriality among Armillaria genets, and provide evidence that rhizomorph systems of more parasitic Armillaria spp. are able to compete effectively with the larger rhizomorph systems of more saprotrophic Armillaria species.