DNA polymerase III (Pol III) is the main component of the E. coli replisome, the multi-protein assembly responsible for DNA replication. Here we present the 1.7 Å crystal structure of a complex between the N-terminal PHP domain of the polymerase subunit α and the C-terminal segment of the proof-reading exonuclease subunit ε. The structure shows that ε is attached to α at a site far from the active site of the polymerase, requiring a long tether for the exonuclease domain to approach the DNA. Nuclear magnetic resonance (NMR) experiments of a reconstituted complex consisting of full-length α, ɛ, θ and a dimer of ß sliding clamp demonstrate that a segment of about 20 residues of ε remains highly mobile in the complex. This segment connects the globular exonuclease domain of ε with its C-terminal α-binding peptide, presenting an unusually long flexible tether. Photo-crosslinking experiments with p-benzoyl-L-phenylalanine incorporated at different sites of the PHP domain of α confirm the conformational variability of the tether.