European (Anguilla anguilla) and American eel (A. rostrata) represent a remarkable case of interspecific hybridization. They are both panmictic and spawn in partial sympatry in the Sargasso Sea, occasionally producing viable, fertile hybrids, primarily found in Iceland. We studied introgressive hybridization from American into European eel based on whole-genome sequences of 78 individuals, encompassing European, American and 21 putative hybrid eels. Previous studies using few genetic markers could not resolve whether hybridization involved simple unidirectional backcrossing or a more complex hybrid swarm scenario. However, local ancestry inference along individual chromosomes revealed Icelandic hybrids were primarily F1 hybrids or first-generation backcrosses toward European eel, with a few showing more complex backcrossing histories. All European eels outside Iceland contained short chromosomal blocks from American eel, indicating a porous genome. We found no evidence for previously stated hypotheses about geographical gradients of introgression in European eel outside Iceland. Several chromosomal regions showed high divergence between the species, but haplotype blocks introgressed from American eel were identified both within and outside these regions. There was little correspondence between regions of high relative and high absolute divergence (d_XY), and they presumably reflect selective sweeps within species or regions of reduced recombination rather than barrier loci. We identified a single genomic region with evidence of introgression from American into European eel at multiple occasions, under positive selection in both species. Thus, although the two species maintain genetic integrity, their gene pools are not independent and represent a common pool of standing variation for future adaptive responses.