Prior to joining the faculty at Harvard in 2015, Allen was UPS Foundation Professor at the Institute for Advanced Study in Princeton, New Jersey.

[14] Allen's grandfather was a Baptist preacher who helped found the first NAACP chapter in North Florida and her great-grandmother was a suffragette.

[5][17] She then matriculated at Princeton University, where she obtained a Bachelor of Arts in classics, summa cum laude, in 1993 with membership in Phi Beta Kappa.

[28] She was the UPS Foundation Professor at the Institute for Advanced Study in Princeton, before joining the Harvard faculty and becoming director of the Safra Center in 2015.

[29] She was named a MacArthur Foundation Fellow in 2001, in recognition of her combining "the classicist's careful attention to texts and language with the political theorist's sophisticated and informed engagement".

[32] Together with Stephen B. Heintz and Eric Liu, Allen chaired the bipartisan Commission on the Practice of Democratic Citizenship of the American Academy of Arts and Sciences.

[34] In October 2022, Allen joined the Council for Responsible Social Media project launched by Issue One to address the negative mental, civic, and public health impacts of social media in the United States co-chaired by former House Democratic Caucus Leader Dick Gephardt and former Massachusetts Lieutenant Governor Kerry Healey.