© 2020 by the authors. Licensee MDPI, Basel, Switzerland. The Phytophthora genus includes some of the most devastating plant pathogens. Here we report draft genome sequences for three ubiquitous Phytophthora species—Phytophthora chlamydospora, Phytophthora gonapodyides, and Phytophthora pseudosyringae. Phytophthora pseudosyringae is an important forest pathogen that is abundant in Europe and North America. Phytophthora chlamydospora and Ph. gonapodyides are globally widespread species often associated with aquatic habitats. They are both regarded as opportunistic plant pathogens. The three sequenced genomes range in size from 45 Mb to 61 Mb. Similar to other oomycete species, tandem gene duplication appears to have played an important role in the expansion of effector arsenals. Comparative analysis of carbohydrate-active enzymes (CAZymes) across 44 oomycete genomes indicates that oomycete lifestyles may be linked to CAZyme repertoires. The mitochondrial genome sequence of each species was also determined, and their gene content and genome structure were compared. Using mass spectrometry, we characterised the extracellular proteome of each species and identified large numbers of proteins putatively involved in pathogenicity and osmotrophy. The mycelial proteome of each species was also characterised using mass spectrometry. In total, the expression of approximately 3000 genes per species was validated at the protein level. These genome resources will be valuable for future studies to understand the behaviour of these three widespread Phytophthora species.