[6] Having won a choral scholarship, she studied English literature at St Catharine's College, Cambridge, graduating with a Bachelor of Arts (BA) degree in 1991.

[6][11][12] Interested in the relationship between poetics and metaphysics, she then moved into philosophical theology and undertook postgraduate studies in this field at the Faculty of Divinity, University of Cambridge.

[11][13] She completed her Doctor of Philosophy (PhD) degree in 1996 with a thesis titled The Sacred Polis: Language, Death and Liturgy.

[17] Pickstock has from the start of her career been associated with the radical orthodoxy movement,[18] on account of her collaboration with John Milbank, her then doctoral supervisor.

[19] Her own academic work is both like and unlike that of her mentor: they are both identifiable as "post-modern critical Augustinian" theologians,[20] heavily influenced by both 20th-century French theory and the Christian Platonic tradition.

Her work also tends to begin more frequently with direct reflection upon the writings of Plato, an engagement she has continued to pursue throughout her career.

The path of return, as Pickstock conceives it, runs through the postmodern (largely French) critique of modernity, then beyond to a non-foundational theology of liturgical encounter—an encounter with being through language.

Building on the foundation of Augustine's treatise De Musica, several of Pickstock's essays have argued that music is “the science that most leads toward theology,"[22] provided it be properly conceived as a contemplative mode of measuring reality.

While certain modern approaches to music, as narrated by Pickstock, have tended to distort its metaphysical character in various ways, certain 20th-century and contemporary composers such as Olivier Messiaen and James MacMillan have opened up possibilities of radical return.

For the form of the other—of anything a person encounters or takes in—will necessarily strike the perceiver differently every time, so that each act of recognition circles back to the other's identity, but in a new way.