Critchley argues that philosophy commences in disappointment, either religious or political. These two axes may be said largely to inform his published work: religious disappointment raises the question of meaning and has to, as he sees it, deal with the problem of nihilism; political disappointment provokes the question of justice and raises the need for a coherent ethics.
Critchley studied philosophy at the University of Essex (BA 1985, PhD 1988,) and at the University of Nice (M.Phil. 1987). Among his teachers were Robert Bernasconi, Jay Bernstein, Frank Cioffi, Dominique Janicaud and Onora O'Neill. His M.Phil. thesis dealt with the problem of the overcoming of metaphysics in Heidegger and Carnap; his Ph.D. dissertation was on the ethics of deconstruction in Emmanuel Levinas and Derrida.
Following a period as a university fellow at Cardiff University, Critchley was appointed a lecturer in philosophy at Essex in 1989, becoming reader in philosophy in 1995, and professor in 1999. He was director of the university's Centre for Theoretical Studies and collaborated closely with Ernesto Laclau. Critchley was president of the British Society for Phenomenology from 1994-99. In 1997 and 2001 he held a Humboldt Research Fellowship in philosophy at Frankfurt. Between 1998-2004, he was a programme director of the College international de philosophie, Paris. In 2006-7 he was a scholar at the Getty Research Institute in Los Angeles. Since 2004 Critchley has been professor of philosophy at the New School for Social Research. He was appointed chair of philosophy in 2008. He has held visiting professorships at numerous universities, including Sydney (2000), Notre Dame (2002), Cardozo Law School (2005) and at the University of Oslo (2006). In 2009 he was appointed a part-time professor of philosophy at Tilburg University in the Netherlands, where he runs a summer school and teaches in philosophy and liberal arts.
Critchley is also a professor of philosophy at the European Graduate School in Saas-Fee, Switzerland.
Critchley is "chief philosopher" of the International Necronautical Society, a semi-fictitious avant-garde network that surfaces through proclamations, "denunciations" and live events. He has collaborated closely with the novelist Tom McCarthy on projects including the society's Declaration on Inauthenticity and their joint publications on Joyce and Shakespeare. At an event at the Tate Britain art gallery two lecturers purporting to be Critchley and McCarthy were, in mischievous keeping with the inauthentic theme, played by actors. The Declaration of Inauthenticity was presented at the opening of the Athens Biennale by Greek actors in June 2009. Critchley also collaborates with American, Jamieson Webster, and French artist, Philippe Parreno.