That same year, she made her Broadway debut in The Lieutenant of Inishmore (2006) earning a Tony Award for Best Featured Actress in a Play nomination.

Pill's other notable stage roles include in Blackbird (2007), Mauritius (2007), The Miracle Worker (2010), The House of Blue Leaves (2011), and Three Tall Women (2018).

Pill had prominent roles in the films Confessions of a Teenage Drama Queen (2004), Plain Truth (2004), Dan in Real Life (2007), Milk (2008), Midnight in Paris (2011), Hail, Caesar!

[2][3] Pill attended Vaughan Road Academy,[4] in its Interact program, designed for studying dance, music, athletics, and theatre.

The next year, she landed a small role in Skipped Parts in 2000 starring Drew Barrymore and Mischa Barton, then appeared in four more TV movies and features that year, including playing Farrah Fawcett's daughter in the TNT network movie Baby and a lead role in the Canadian film The Dinosaur Hunter, which was originally intended to be shown at a dinosaur museum and on a provincial education channel, but which made its way to the Burbank International Film Festival, winning Pill an award for Best Child Actress.

Since graduating from high school, Pill moved to New York to pursue a career in theatre, but continued to work in movies such as Dan in Real Life in 2007.

She returned to Broadway in the Theresa Rebeck play Mauritius (2007) acting alongside F. Murray Abraham, Bobby Cannavale, and Dylan Baker.

[8] John Lahr of The New Yorker praised Pill describing her as "excellent" adding, "It says something about the appeal of Alison Pill—an actress with a big future—that her compelling combination of ferocity and fragility carries the audience beyond the inconsistencies of the story.

"[9] That same year she acted in the Manhattan Theatre Club production of the David Harrower play Blackbird starring alongside Jeff Daniels.

In 2009 she replaced Elliot Page in a role in Jack & Diane[13] but due to postponement of the project neither ended up in it by the time it ran in 2012.

She's no less convincing as 20-year-old Boston-Irish Sullivan, hired in 1887 by the Keller family in Alabama to serve as governess to Helen, left deaf and blind by an illness in her infancy".

[15] The following year she acted in another Broadway revival, the John Guare play The House of Blue Leaves with Ben Stiller, Edie Falco, Jennifer Jason Leigh, and Thomas Sadoski.

[20] From 2012 until its ending in 2014, she was in the HBO political drama series The Newsroom portraying journalist Maggie Jordan at a fictional cable news show.

[33] David Cote of The Observer hailed her performance writing, "Pill proves to be the evening's MVP" adding, "[She] embodies that brokenness with a palpable heat I wish could have ignited everything around her".

Baruchel made their engagement public when he thanked Pill as his fiancée during an acceptance speech at the Genie Awards in Ottawa, Ontario.