Human ubiquitin ligase HERC2, a component of the DNA repair machinery, has been linked to neurological diseases and cancer. Here, we show that the ZZ domain of HERC2 (HERC2_ZZ) binds to histone H3 tail and tolerates posttranslational modifications commonly present in H3. The crystal structure of the HERC2_ZZ:H3 complex provides the molecular basis for this interaction and highlights a critical role of the negatively charged site of HERC2_ZZ in capturing of A1 of H3. NMR, mutagenesis, and fluorescence data reveal that HERC2_ZZ binds to H3 and the N-terminal tail of SUMO1, a previously reported ligand of HERC2_ZZ, with comparable affinities. Like H3, the N-terminal tail of SUMO1 occupies the same negatively charged site of HERC2_ZZ in the crystal structure of the complex, although in contrast to H3 it adopts an α-helical conformation. Our data suggest that HERC2_ZZ may play a role in mediating the association of HERC2 with chromatin.