Although the evolutionary response to random genetic drift is classically modelled as a sampling process for populations with fixed abundance, the abundances of populations in the wild fluctuate over time. Furthermore, since wild populations exhibit demographic stochasticity and since random genetic drift is in part due to demographic stochasticity, theoretical approaches are needed to understand the role of demographic stochasticity in eco-evolutionary dynamics. Here we close this gap for quantitative characters evolving in continuously reproducing populations by providing a framework to track the stochastic dynamics of abundance density across phenotypic space using stochastic partial differential equations. In the process we develop a set of heuristics to operationalize the powerful, but abstract theory of white noise and diffusion-limits of individual-based models. Applying these heuristics, we obtain stochastic ordinary differential equations that generalize classical expressions of ecological quantitative genetics. In particular, by supplying growth rate and reproductive variance as functions of abundance densities and trait values, these equations track population size, mean trait and additive genetic variance responding to mutation, demographic stochasticity, random genetic drift, deterministic selection and noise-induced selection. We demonstrate the utility of our approach by formulating a model of diffuse coevolution mediated by exploitative competition for a continuum of resources. In addition to trait and abundance distributions, this model predicts interaction networks defined by niche-overlap, competition coefficients, or selection gradients. Using a high-richness approximation, we find linear selection gradients and competition coefficients are uncorrelated, but magnitudes of linear selection gradients and quadratic selection gradients are both positively correlated with competition coefficients. Hence, competing species that strongly affect each other’s abundance tend to also impose selection on one another, but the directionality is not predicted. This approach contributes to the development of a synthetic theory of evolutionary ecology by formalizing first principle derivations of stochastic models tracking feedbacks of biological processes and the patterns of diversity they produce.