ABSTRACT Ecological restoration has emerged as a prominent conservation and management strategy widely touted for its utility in evaluating ecological theories when designed experimentally. In comparison, restoration has been underutilized to investigate evolution‐oriented questions, despite the importance of evolutionary processes in conservation and management settings. Here, we leverage an experimental restoration approach using the eastern oyster, Crassostrea virginica , an economically valuable and ecologically important reef‐building foundation species. Previous small‐scale manipulations of oyster source identity highlight the potential evolutionary implications of sources used in restoration, yet have rarely been empirically evaluated at the scale of a restored reef. We sourced juvenile oysters from four commercial hatcheries spanning a broad geographic range along the Atlantic coast of the United States to build restored oyster reefs of diverse initial source composition in a single New England estuary. We characterized four distinct genetic clusters associated with hatchery source using SNP genotyping data and examined whether the frequencies of these genetic clusters on our mixed reefs shifted over the course of our restoration experiment. We documented strong shifts in the relative abundance of certain genetic lineages, consistent with differential mortality among oyster sources. Further, we found significant variation in ecologically relevant traits, including multi‐parasite infection patterns and oyster size, associated with source identity. Oyster condition index, a commonly used proxy for oyster health, was associated with higher relative mortality over time. Our research highlights how evolutionary processes can influence restoration demographics and how, concurrently, restoration can serve as a powerful platform for gaining fundamental, and sometimes unexpected, insights into eco‐evolutionary dynamics.