Blastocystis is one of the most prevalent eukaryotes in the gut, yet its role remains contested: pathogen, passenger, or partner. Drawing on our COST Action’s One Health programme—spanning humans, animals, and environmental reservoirs—I will synthesise evidence from prevalence surveys, longitudinal cohorts, targeted culturing, and emerging single-cell and microfluidic assays. Together, these data support a context-dependent model in which phenotype reflects subtype/strain identity interacting with host ecology: diet and fibre intake, microbiome state, immune tone, and environmental exposure. I will present four converging signals: (i) frequent carriage in healthy populations; (ii) subtype-specific associations with increased bacterial diversity and fermentation capacity; (iii) experimental hints of trophic interactions—including digestion of bacteria in vitro—that may rewire community structure; and (iv) plausible transmission links across humans, livestock, and water. Building on this, I propose practical “rules of engagement” that predict when Blastocystis behaves as a commensal ally versus a clinical risk, and outline minimum reporting and screening standards relevant to faecal microbiota transplantation donors. Methodologically, I will highlight open, strain-resolved diagnostics beyond conventional PCR/sequencing, interoperable subtyping nomenclature and metadata via a living BlastoDB, and integrated multi-omics with high-frequency sampling (stool, diet logs, saliva/urine metabolomics, and wearables). Finally, I will test a provocative hypothesis: that Blastocystis may act as an early ecosystem engineer—or thrive as a beneficiary—during gut community assembly. By replacing anecdotes with validated rules, we can move toward protist-guided strategies for maintaining gut and environmental health across species.