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The ability of scleractinian corals to thrive in the oligotrophic (low-nutrient, low-productivity) surface waters of the tropical ocean is commonly attributed to their symbiotic relationship with photosynthetic dinoflagellates1,2. The evolutionary history of this symbiosis might clarify its organismal and environmental roles. It is currently unclear whether photosymbiosis first arose in the Triassic, with the emergence of scleractinian corals, or if it was already prevalent amongst older coral groups that have since gone extinct3–5. Here, we report the first measurements of nitrogen isotope ratios of coral-bound organic matter (CB-δ15N) in samples from Mid-Devonian reefs (Givetian, ca. 385 Ma), which represent the oldest isotopic constraint on the evolution of photosymbiosis to date. The colonial tabulate and loosely colonial (dendroid) corals analyzed have low CB-δ15N values (1.59‰±0.53‰ and 1.45±0.66‰, respectively) in comparison with co-occurring solitary rugose corals (4.38‰±1.34‰). The isotopic difference between Devonian colonial and solitary corals (2.86‰±0.86‰) is statistically indistinguishable from that observed between modern symbiont-bearing and symbiont-barren corals (3.38‰±1.05‰). From this evidence we infer that Mid-Devonian colonial tabulate and loosely colonial (dendroid) corals hosted active photosymbionts, while solitary rugose corals did not. The low CB-δ15N values of the Devonian colonial tabulate and dendroid corals relative to the modern range suggest that Devonian reefs formed in biogeochemical regimes analogous to the modern oligotrophic subtropical gyres. Widespread oligotrophy during the Devonian likely may have promoted coral photosymbiosis, potentially explaining why Devonian reefs were the most productive reef ecosystems of the Phanerozoic.