Background: Mounting evidence supports metastatic ablation for oligometastatic prostate cancer (OMPC). Importantly, biomarkers to determine patients who benefit most from complete ablation are unknown. We hypothesize that stereotactic ablative radiation (SABR) will improve oncologic outcomes in men with OMPC. Methods: In this phase II randomized trial, men with recurrent hormone-sensitive OMPC (1-3 radiation fields) were stratified by primary management (radiotherapy vs surgery), PSA doubling time, and prior androgen deprivation therapy and randomized 2:1 to SABR or observation (OBS). The primary endpoint was progression at 6 months by PSA (≥ 25% increase and ≥ nadir + 2 ng/mL), conventional imaging (RECIST 1.1 criteria or new lesion on bone scan), or symptomatic decline. Tissue, liquid and imaging correlatives were analyzed as biomarkers. Results: From 5/2016-3/2018, 54 patients were randomized. Progression at six months occurred in 19% of SABR patients and 61% of observation patients [p=0.005]. SABR improved median PFS (not reached vs 5.8 months, HR 0.30, p = 0.0023). Total consolidation of PSMA radiotracer-avid disease decreased the risk of new lesions at six months (16% vs 63%, p = 0.006). No toxicity ≥ grade 3 was observed. T-cell receptor sequencing identified increased clonotypic expansion (p = 0.03) following SABR and correlation between baseline clonality and progression with SABR only. Analysis of circulating tumor DNA (ctDNA) and germline mutations identified a mutation profile that was associated with benefit from SABR. Conclusions: SABR for OMPC improves outcomes and is enhanced by total consolidation of disease identified by PSMA-targeted PET. SABR induces a systemic immune response, and baseline immune phenotype and tumor mutation status may predict the benefit from SABR. These results underline the importance of prospective randomized investigation of the oligometastatic state with integrated imaging and biological correlates. Clinical trial information: NCT02680587