In this work, we have investigated the evolutionary dynamics of a generalist pathogen, e.g., a virus population, that evolves toward specialization in an environment with multiple host types. We have particularly explored under which conditions generalist viral strains may rise in frequency and coexist with specialist strains or even dominate the population. By means of a nonlinear mathematical model and bifurcation analysis, we have determined the theoretical conditions for stability of nine identified equilibria and provided biological interpretation in terms of the infection rates for the viral specialist and generalist strains. By means of a stability diagram, we identified stable fixed points and stable periodic orbits, as well as regions of bistability. For arbitrary biologically feasible initial population sizes, the probability of evolving toward stable solutions is obtained for each point of the analyzed parameter space. This probability map shows combinations of infection rates of the generalist and specialist strains that might lead to equal chances for each type becoming the dominant strategy. Furthermore, we have identified infection rates for which the model predicts the onset of chaotic dynamics. Several degenerate Bogdanov–Takens and zero-Hopf bifurcations are detected along with generalized Hopf and zero-Hopf bifurcations. This manuscript provides additional insights into the dynamical complexity of host–pathogen evolution toward different infection strategies.