We examined the local adaptation patterns in a system comprising several interconnected heterogeneous plant populations from which populations of two phylogenetically closely related pathogens were also sampled. The host is Hordeum vulgare (cultivated barley); the pathogens are Pyrenophora teres f. teres (net form) and Pyrenophora teres f. maculata (spot form), the causal agents of barley net blotch. We integrated two approaches, the comparison between the population structures of the host and the pathogens, and a cross-inoculation test. We demonstrated that two closely related pathogens with very similar niche specialisation and life-styles can give rise to different co-evolutionary outcomes on the same host. Indeed, we detected local adaptation for the net form of the pathogen but not for the spot form. We also provided evidence that an a-priori well-known resistance quantitative-trait-locus on barley chromosome 6H is involved in the co-evolutionary ‘arms race’ between the plant and the net-form pathogen. Moreover, data suggested latitudinal clines of host resistance and that different ecological conditions can result in differential selective pressures at different sites. Our data are of interest for on-farm conservation of plant genetic resources, as also in establishing efficient breeding programs and strategies for deployment of resistance genes of P. teres.