Most organisms exist in complex ecological communities, in which they encounter and interact with many other species, often simultaneously. Despite the fact that organisms evolve in and respond to complex ecological communities, most research on species interactions focuses on pairwise interactions between two species (e.g. host and a pathogen). This reductionism is partly borne from experimental tractability – it is simply easier to observe or manipulate smaller numbers of organisms. A focus on pairwise systems has revealed invaluable knowledge on the ecology and evolution of species interactions. However, it is becoming increasingly clear that the outcomes of pairwise interactions studied in this fashion commonly fail to predict the ecological and evolutionary changes that occur between species when they interact in more complex ecological contexts. The goal of my dissertation research was to address this knowledge gap and advance our understanding of the evolutionary ecology of multi-species interactions. Research on host-parasite interactions is dominated by a focus on tightly co-evolved species pairs between a specialized parasite and its host. However, a large number, and maybe even the majority, of parasites are capable of infecting multiple hosts. Whether, and to what degree, the evolutionary dynamics that characterize specialized interactions also apply to diffuse interactions between generalist parasites and their many host taxa is an important, and largely unanswered question. In Chapter 2, I present work exploring how a generalist plant parasite evolves in response to the heterogenous selection pressures they face when infecting the diversity of host species that they encounter. Interestingly, I found that this heterogenous selection pressure by different host taxa can generate signatures of balancing selection, which is the same genomic footprint of selection that is expected in negative frequency dependent selection, also referred to as Red Queen coevolution. In a second set of projects, I investigated how resource exchange in the keystone mutualism between legumes and rhizobia is affected when the host plant is infected with a common plant parasite. Parasitism has been observed to influence the fitness outcomes of mutualisms, however, the specific traits the mediate fitness outcomes in mutualisms have been rarely studied. In chapter 3, I developed a set of trait measurements to quantify resource exchange between interacting partners and found that variation in these traits is sensitive to both plant and rhizobia genotype. In Chapter 4, I show that resource exchange traits shift in response to parasitism, but in a genotype dependent manner. This finding highlights that (1) indirect effects on resource exchange may be an important and underappreciated consequence of parasitism and (2) resource exchange traits may exhibit standing variation that could be acted on by natural selection. Future work is needed to quantify the heritability of key mutualism traits and whether how selection acts on these traits across ecological contexts.