The DNA target/ligand conjugates (HLX, X = Pn and Mn, n = 1–3) were synthesized where various lengths of −CONH(CH2CH2O) n CH2CH2NHCO– linkers with a 9-phenanthrenyl (P) or methyl (M) terminal as DNA targets replace the methyl group of 2,6-di(amide-tether cyclen)-p-cresol ligand (HL). DNA binding, DNA cleavage, cellular uptake, and cytotoxicity of [Cu2(μ-OH)(LX)](ClO4)2 (1X ) are examined and compared with those of [Cu2(μ-OH)(L)](ClO4)2 (1) to clarify roles of DNA targets. Upon reaction of 1X with H2O2, μ-1,1-O2H complexes are formed for DNA cleavage. 1P1 , 1P2 , and 1P3 are 22-, 11-, 3-fold more active for conversion of Form II to III in the cleavage of supercoiled plasmid DNA with H2O2 than 1, where the short P-linker may fix a dicopper moiety within a small number of base pairs to facilitate DNA double-strand breaks (dsb). This enhances the proapoptotic activity of 1P1 , 1P2 , and 1P3 , which are 30-, 12-, and 9.9-fold cytotoxic against HeLa cells than 1. DNA dsb and cytotoxicity are 44% correlated in 1P1–3 but 5% in 1M1–3 , suggesting specific DNA binding of P-linkers and nonspecific binding of M-linkers in biological cells. 1P1–3 exert cancer cell-selective cytotoxicity against lung and pancreas cancer and normal cells where the short P-linker enhances the selectivity, but 1M1–3 do not. Intracellular visualization, apoptosis assay, and caspase activity assay clarify mitochondrial apoptosis caused by 1P1–3 . The highest cancer cell selectivity of 1P1 may be enabled by the short P-linker promoting dsb of mitochondrial DNA with H2O2 increased by mitochondrial dysfunction in cancer cells.