Flanagan is the inaugural chair holder of the Sherman Fairchild Distinguished Professorship in Digital Humanities at Dartmouth College, where she has served since 2008.

[4] Awards Residencies and Visiting Fellowships Faculty Appointments Talks Flanagan has given keynotes to the Association of Professional Futurists[15] and the Games Learning and Society Conference.

[18][19] re:skin (MIT Press, 2007), a book Flanagan edited With Austin Booth, is a collection of fiction and theory exploring technology, interfaces, and the body.

Simulacri (SIMilarities, Symbols, Simulacra) (Edizioni Unicopli, 2003), a book she co-authored with Matteo Bittanti, investigates the fan culture of The Sims.

Finally, Reload: Rethinking Women and Cyberculture (MIT Press, 2002)[21] was also co-edited with Austin Booth and addresses gender issues in both fictional and real-life cyber-culture.

Values at Play in Digital Games (MIT Press, 2014) with Helen Nissenbaum features a collection of guest writers including Frank Lantz, Celia Pearce, and Tracy Fullerton.

Resonym designed and published Buffalo: The Name Dropping Game, Awkward Moment, Monarch and VISITOR in Blackwood Grove.

Her artwork has exhibited internationally at The Whitney Museum of American Art, SIGGRAPH, Ars Electronica, The Guggenheim, and Turbulence.org.

In Grace's origin story she first examines thousands of images of Mary Shelley's monster, Frankenstein, and then applies her learning of a female art history to the creation of portraits of her "father figure".

The work used computational neuroscience to show how beliefs people have about facial features can be related to culture and identity.

[borders] has since been exhibited in several locations including the Museum of Art, Architecture and Technology in Lisbon, Portugal in October 2019, the Museum of Fine Arts in Cologne from 2017 to 2018, and the Electronic Language International Festival in 2014. xyz (2009) combined Flanagan's interests in virtual environments and interactive writing, allows participants to build poetry in 2-dimensional game worlds.

She studied film for her undergraduate and masters work while her PhD was in Computational Media focusing on game design.