The success of non-native species (NNS) invasions depends on patterns of dispersal and connectivity, which underpin genetic diversity, population establishment and growth. In the marine environment, both global environmental change and increasing anthropogenic activity can alter hydrodynamic patterns, leading to significant inter-annual variability in dispersal pathways. Despite this, multi-generational dispersal is rarely explicitly considered in attempts to understand NNS spread or in the design of management interventions. Here, we present a novel approach to quantifying species spread that considers range expansion and network formation across time using the non-native Pacific oyster, Magallana gigas (Thunberg 1793), as a model. We combined biophysical modelling, dynamic patch occupancy models, consideration of environmental factors, and graph network theory to model multi-generational dispersal in northwest Europe over 13 generations. Results revealed that M. gigas has a capacity for rapid range expansion through the creation of an ecological network of dispersal pathways that remains stable through time. Maximum network size was achieved in four generations, after which connectivity patterns remained temporally stable. Multi-generational connectivity could therefore be divided into two periods: network growth (2000−2003) and network stability (2004–2012). Our study is the first to examine how dispersal trajectories affect the temporal stability of ecological networks across biogeographic scales, and provides an approach for the assignment of site-based prioritisation of non-native species management at different stages of the invasion timeline. More broadly, the framework we present can be applied to other fields (e.g. Marine Protected Area design, management of threatened species and species range expansion due to climate change) as a means of characterising and defining ecological network structure, functioning and stability.