Abundant ecological opportunity is thought to drive adaptation and diversification. The presence of multiple opportunities leads to divergent selection, which can slow adaptation when niche-specific beneficial mutations have antagonistically pleiotropic effects. Alternately, competition for multiple opportunities can generate divergent selection leading to high rates of adaptive differentiation. Which outcome occurs may depend on the spatial structure of those ecological opportunities. In a mixture of resources, competition for multiple opportunities can drive divergent selection; however if each resource is available in a spatially distinct patch, competition for multiple opportunities simultaneously cannot occur. We report the effects of extent and spatial structure of ecological opportunity on the evolutionary dynamics of populations of Pseudomonas fluorescens over 1000 generations. We varied extent of ecological opportunity by varying the number of sugar resources (mannose, glucose, and xylose), and varied spatial structure by providing resources in either mixtures, or spatially distinct patches. We saw that a particularly novel resource (xylose) drove the rate of adaptation when in a mixture but had no effect on diversity. Instead we saw the evolution of a single adaptive strategy that differed with respect to phenotype and degree of specialization, depending on both the extent and spatial structure of ecological opportunity.