The history of life on Earth has been shaped by a series of major evolutionary innovations. While some of these innovations occur repeatedly, some of the most important innovations are evolutionary singularities, arising only once. This fact has often been interpreted to mean that singularities are particularly difficult, low-probability evolutionary events, implying the long-term course of life on Earth is highly contingent. Alternatively, singularities could arise from evolutionary priority effects, where first-movers suppress subsequent independent origins. Here, we disentangle these hypotheses by examining the origins of phototrophy. The ability to use light for energy evolved independently twice, preserving information about their origins that is lost when examining singularities. We show that the two forms of phototrophy occupy opposite ends of key trade-offs: most importantly efficiency of light capture vs. return on investment. Our results suggest that the dual singularity of phototrophy exists due to evolutionary interactions between nascent phototrophs, within a phototrophic niche space too large for a single first mover to fill all niches and fully suppress all future innovation. While often ignored over geological time scales, ecological interactions and evolutionary priority effects may play a fundamental role in the tempo and mode of major evolutionary innovations.