Bacterial adaptation proceeds predominantly through horizontal gene transfers (HGTs). Often, the evolution of a new phenotype (such as the ability to grow on a new set of nutrients) requires the acquisition of multiple DNA segments. It is unlikely that these are acquired via HGT simultaneously. Thus, the first HGT event is either neutral and becomes beneficial only after the second HGT event, or it provides a benefit by itself in another environment and thus represents an exaptation for the second adaptation. In this work, we studied the metabolic networks of 53 E. coli strains and their ancestors. Using flux balance analysis to define metabolic phenotypes, we found that (i) in contrast to expectations from a neutral model of HGT, new phenotypes acquired along a single phylogenetic branch are less likely to require the acquisition of multiple DNA segments than expected in a neutral model; (ii) new phenotypes acquired relative to a more distant ancestor often relied on multiple HGT events spread over different phylogenetic branches; and (iii) this split of the acquisition of adaptive gene sets over several phylogenetic branches was more frequent than expected from a neutral model of HGT. We conclude that exaptation is widespread in metabolic adaptation of E. coli strains.