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Light‐activated ruthenium polypyridyl anticancer prodrugs often suffer from poor water solubility, poor selectivity, and/or ill‐defined intracellular targets. Coordination of the  d ‐ or  l ‐glucose thioether ligand  3  (2‐(2‐(2‐(methylthio)ethoxy)ethoxy)ethyl‐β‐glucopyranoside) to the highly lipophilic ruthenium complex [Ru(tpy)(dppn)(H 2 O)] 2+  ([ 1 ] 2+ ; dppn=benzo[ i ]dipyrido‐[3,2‐ a :2′,3′‐ c ]phenazine, tpy=2,2′:6′,2′′‐terpyridine) solved all these problems at once. The two enantiomers of [Ru(tpy)(dppn)( 3) ][PF 6 ] 2 , [ d ‐ 2 ][PF 6 ] 2  and [ l ‐ 2 ][PF 6 ] 2 , were soluble in water, which allowed the influence of the chirality of the glucose moiety on uptake, toxicity, and intracellular localization of the prodrug to be probed without changing any other physicochemical properties. Both compounds showed mild, but different, cytotoxicity in A549 (human lung carcinoma) and MCF‐7 (human breast adenocarcinoma) cancer cells in the dark, whereas following low doses of visible light irradiation (3.1 J cm −2  at  λ  = 454 nm), a similar, but high cytotoxicity (EC 50  < 1 μ m ), was observed. Irrespective of the chirality, both slightly emissive Ru complexes were found in the mitochondria, and two modes of action may contribute to light‐induced cell death: 1) the glucose thioether ligand is photosubstituted by water, thus [ 1 ] 2+ , which interacts with DNA at an exceptionally high 400:1 base pair/Ru ratio, is released; 2) both [ 1 ] 2+  and [ 2 ] 2+  produce massive amounts of singlet oxygen, which leads to very efficient photodynamic DNA cleavage.

d ‐ Versus l ‐Glucose Conjugation: Mitochondrial Targeting of a Light‐Activated Dual‐Mode‐of‐Action Ruthenium‐Based Anticancer Prodrug