Phytophthora cinnamomi, the causal agent of Phytophthora root rot, is a cosmopolitan plant pathogen with a wide host range that threatens native ecosystems and major agricultural crops including avocado. Despite the importance of this invasive alien pathogen, the number of genomic resources for P. cinnamomi are minimal and mechanisms for generating novel genetic diversity remain unclear. Many P. cinnamomi populations have been described as clonal, however despite the lack of sexual reproduction, P. cinnamomi is notorious for its ability to adapt to novel environments and stressors while exhibiting genotypic and phenotypic variability. We generated novel genomic resources for two representative P. cinnamomi isolates to elucidate mechanisms for generating novel genetic diversity and uncover host infection strategies. With these genomic resources we uncovered the genetic and phenotypic variability of P. cinnamomi populations affecting avocado in California and Mexico. The results of this dissertation are presented in two chapters: 1) genomic analyses of two genotypically and phenotypically distinct isolates of P. cinnamomi and transcriptomic analyses of P. cinnamomi infecting various host plants over time; 2) characterizing the phenotypic and genotypic variability of P. cinnamomi populations affecting avocado in California and Mexico. Novel de novo genome assemblies supported by flow cytometry genome size estimations were generated for two representative P. cinnamomi isolates from California avocado. Genomic analyses revealed expanded genome size with complex profile, a bipartite “two-speed” architecture, high synteny between the two isolates, orthologous proteins, and variation in secretome and effector repertoire sizes. Transcriptomic analysis of P. cinnamomi infecting Nicotiana benthamiana, Persea americana and Arabidopsis thaliana revealed host-specific and common in planta gene expression patterns. Population structure analyses revealed that the P. cinnamomi isolates from California and Mexico are clonal and Mexico was likely the source of an introduction event into Southern California avocado growing regions. The P. cinnamomi population from California were less diverse than the population from Mexico and these populations likely belong to the two panglobal lineages of A2 P. cinnamomi. Phenotypic characterization of select isolates revealed variability in fungicide sensitivity, in vitro growth rate, sensitivity to higher growth temperature and virulence in avocado seedlings and pears, despite clonality.