Non‐native species that act as ecosystem engineers – creating new or reintroducing former habitats – challenge perceptions in conservation and restoration. In the wake of the loss of oyster reefs worldwide, non‐native Pacific oysters (Magallana gigas) are now spreading extensively across the former distributions of native reef‐building oyster species. Here, we show that the coastal expansion of Pacific oysters (approximately 1000 km per year) is occurring across the eradicated distribution (>100,000 km) of native oysters. Where Pacific oysters build reefs, they create conspicuous challenges and opportunities for society. Although their reefs alter benthic habitats and often displace native species, Pacific oysters are one of the world’s most valuable aquaculture species, and they also provide numerous ecosystem services. Whether Pacific oysters are the forerunners of habitat regeneration will challenge natural resource management as well as policy making, as coastal communities weigh the pros and cons of embracing or removing this non‐native species.