[4][5] Cunningham began her legal career as a law clerk to Judge Timothy B. Dyk of the United States Court of Appeals for the Federal Circuit from 2001 to 2002.

In 2002, she joined the Chicago office of Kirkland & Ellis as an associate, and was elevated to partner in 2007, where she remained until 2014.

From 2014 to 2021, she was a partner at Perkins Coie in Chicago, where she was a member of the patent litigation practice and served on the 17-member executive committee of the firm.

President Biden nominated Cunningham to the seat vacated by Judge Evan Wallach, who assumed senior status on May 31, 2021.

[15] On January 28, 2022, following Justice Stephen Breyer's announcement of his intention to retire as an associate justice of the U.S. Supreme Court, Cunningham was mentioned as one of the potential nominees for a Supreme Court appointment by President Joe Biden.