Hunicke began her career at Electronic Arts where she worked on multiple games including MySims as Lead Designer and Boom Blox and its sequel as a Producer.

After its completion, Hunicke joined Tiny Speck to develop the social MMORPG Glitch, teaming with Katamari Damacy creator and personal friend Keita Takahashi.

Prior to the release of Glitch, Hunicke left Tiny Speck to co-found Funomena together with Martin Middleton, former teammate and engineer at thatgamecompany.

[12][13] After the release of Journey, Hunicke left thatgamecompany to join Tiny Speck to continue development of their social MMORPG Glitch.

In March 2022, allegations were made by anonymous former employees in a YouTube video released by People Make Games that Hunicke had emotionally abused Funomena staff, bringing up sensitive information about their personal lives during workplace discussions regarding performance.

[4][5] Hunicke later acknowledged this in a now-deleted series of tweets stating that she was sorry that people were hurt by her mistakes and was taking a break but did not respond to any specific contents of the report.

[22] Many successful games have made their first public appearance at the session, including Jonathan Blow's Braid and Valve's Portal.

[27] From 2001 to 2004,[28] Hunicke, Marc LeBlanc, and Robert Zubek created the Mechanics-Dynamics-Aesthetics framework to focus and improve game analysis.

The framework categorizes the many aspects of a game as Mechanics, Dynamics, or Aesthetics, and outlines the inverse perspectives of designer and player.