Outbreaks caused by asexual lineages of fungal and oomycete pathogens are an expanding threat to crops, wild animals and natural ecosystems (Fisher et al. 2012, Kupferschmidt 2012). However, the mechanisms underlying genome evolution and phenotypic plasticity in asexual eukaryotic microbes remain poorly understood (Seidl and Thomma 2014). Ever since the 19th century Irish famine, the oomycete Phytophthora infestans has caused recurrent outbreaks on potato and tomato crops that have been primarily caused by the successive rise and migration of pandemic asexual lineages (Cooke et al. 2012, Yoshida et al. 2013, Yoshida et al. 2014). Here, we reveal patterns of genomic and gene expression variation within a P. infestans asexual lineage by compared sibling strains belonging to the South American EC-1 clone that has dominated Andean populations since the 1990s (Forbes et al. 1997, Oyarzun et al. 1998, Delgado et al. 2013, Yoshida et al. 2013, Yoshida et al. 2014). We detected numerous examples of structural variation, nucleotide polymorphisms and gene conversion within the EC-1 clone. Remarkably, 17 genes are not expressed in one of the two EC-1 isolates despite apparent absence of sequence polymorphisms. Among these, silencing of an effector gene was associated with evasion of disease resistance conferred by a potato immune receptor. These results highlight the exceptional genetic and phenotypic plasticity that underpins host adaptation in a pandemic clonal lineage of a eukaryotic plant pathogen.