A scarcity of favourable habitats and introgression from exotic cultivars are two major threats to black poplars (Populus nigra L.) in Europe. Natural vegetative propagation contributes to maintenance of the species in areas where seedling recruitment is limited. Exhaustive sampling of all mature trees in a natural P. nigra stand (413 individuals at recorded positions), genotyping at 11 SSR loci, and a standardized analysis framework resulted in a precise description of clonality in terms of (a) frequency, (b) spatial growth form, and (c) impacts on the overall spatial genetic structure (SGS). The high proportion of replicated genotypes detected resulted in a genotypic richness (R) of 0.47. Up to 18 ramets were found per multilocus lineage (MLL), but 95% of MLLs contained fewer than five ramets (Pareto index β = 1.07). No significant difference in vegetative propagation potential was found between genders. Uneven spatial distribution of ramets, with clustering of clonal ramets (aggregation index A c = 0.62) and near-zero intermingling between MLLs (clonal dominance index D c = 0.99), resulted in a ‘phalanx’ clonal growth form, explaining most of the SGS observed over short distances (0–20 m, Sp = 0.0324). Although they did not exhibit the typical columnar shape of the Lombardy poplar (P. nigra var. italica), five trees were found to be probable F1 hybrids of this old and widely distributed cultivar.