Born in 1946 in Metz, he has successively been deputy director of the Ecole nationale supérieure des Beaux-Arts in Paris (1979–1982), manager of the Musée national d’art moderne (1982–1985), cultural events representative for the City of Paris (1985–1991), cultural affairs director for the City of Paris (1992–1996), and director of the Georges Pompidou Centre (1996–2002). In May 2002 he was appointed Minister for Culture and Communication, a position he would occupy until March 2004.
In April 2005 he was chosen as general director and president of TV5 Monde and president of Transtélé CanalFrance International (CFI). Jean-Jacques Aillagon left these positions in April 2006 to accept François Pinault’ s offer to become Palazzo Grassi’s general director.

Under his guidance, Palazzo Grassi has presented the first exhibitions dedicated to the François Pinault Collection – "Where Are We Going? Selections from the François Pinault Collection", "The François Pinault Collection, a Post-Pop Selection" and "Sequence 1, Painting and Sculpture in the François Pinault Collection" – as well as a modern art exhibition entitled Picasso, la joie de vivre, 1945-1948. It is under his guidance, as well, that Palazzo Grassi was granted the concession to operate the Punta della Dogana in Venice due to become the Punta della Dogana Centre for Contemporary Art - François Pinault Foundation.

In June 2007 Jean-Jacques Aillagon left his duties as Palazzo Grassi’s director to become the President of the Etablissement public du musée et du domaine national de Versailles. Nevertheless, his contribution to Palazzo Grassi’s adventure continued: he has been the chief curator of the Rome and the Barbarians, the Birth of a New World historical exhibition (january - july 2008).