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Além de sua carreira no teatro, John apareceu em vários filmes, incluindo os musicais De-Lovely (2004) e Os Produtores (2005). Antes de trabalhar na televisão britânica, ele apareceu nos seriados estadunidenses Titans e Central Park West. No Reino Unido, trabalhou como ator e apresentador na BBC (CBBC), no seu autoproduzido programa de entretenimento Tonight's the Night, e no papel de Jack Harkness, das séries Doctor Who e Torchwood, pelo qual foi indicado ao BAFTA Cymru (a versão galesa do BAFTA).
De 2012 até o momento, John desempenha o papel do vilão Malcolm Merlyn / Ra's Al Ghul na série Arrow.
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