The decline of the European oysterOstrea edulisacross its biogeographic range has been driven largely by over-fishing and anthropogenic habitat destruction, often to the point of functional extinction. However, other negatively interacting factors attributing to this catastrophic decline include disease, invasive species and pollution. In addition, a relatively complex life history characterized by sporadic spawning rendersO. edulisbiologically vulnerable to overexploitation. As a viviparous species, successful reproduction inO. edulispopulations is density dependent to a greater degree than broadcast spawning oviparous species such as the Pacific oysterCrassostrea(Magallana)gigas. Here, we report on the benthic assemblage ofO. edulisand the invasive gastropodCrepidula fornicataacross three actively managed South coast harbors in one of the few remainingO. edulisfisheries in the UK. Long-term data reveals that numbers ofO. edulissampled within Chichester Harbour have decreased by 96%, in contrast numbers ofC. fornicatasampled have increased by 441% over a 19-year period. The recent survey data also recorded extremely low densities ofO. edulis,and extremely high densities ofC. fornicata, within Portsmouth and Langstone Harbours. The native oyster’s failure to recover, despite fishery closures, suggests competitive exclusion byC. fornicatais preventing recovery ofO. edulis, which is thought to be due to a lack of habitat heterogeneity or suitable settlement substrate. Large scale population data reveals that meanO. edulisshell length and width has decreased significantly across all years and site groups from 2015 to 2017, with a narrowing demographic structure. An absence of juveniles and lack of multiple cohorts in the remaining population suggests that the limited fishing effort exceeds biological output and recruitment is poor. In the Langstone & Chichester 2017 sample 98% of the population is assigned to a single cohort (modal mean 71.20 ± 8.78 mm, maximum length). There is evidence of small scale (<5 km) geographic population structure between connected harbors; the 2015 Portsmouth and Chichester fishery populations exhibited disparity in the most frequent size class with 36% within 81–90 mm and 33.86% within 61–70 mm, respectively, the data also indicates a narrowing demographic over a short period of time. The prevalence of the disease Bonamiosis was monitored and supports this microgeographic population structure. Infection rates ofO. edulisbyBonamia ostreaewas 0% in Portsmouth Harbor (n= 48), 4.1% in Langstone (n= 145) and 21.3% in Chichester (n= 48) populations. These data collectively indicate thatO. edulisis on the brink of an ecological collapse within the Solent harbors. Without effective intervention to mitigate the benthic dominance byC. fornicatain the form of biologically relevant fishery policy and the management of suitable recruitment substrate these native oyster populations could be lost.