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In 2015, Aycox released her debut EP, Red Velvet Room, which contained five songs of her own original music.

In July 2009, Aycox began to portray the character Jaimie Allen (an undercover LAPD police officer) in the TNT action/drama series Dark Blue. It ended its run on September 15, 2010.

In 2007, Aycox appeared in the thriller movie Perfect Stranger, alongside Halle Berry and Bruce Willis, as a woman trying to blackmail a wealthy advertising executive. The following year, Aycox was in The X-Files: I Want to Believe, the second feature film installment of The X-Files franchise. Filming began in December 2007 and finished on March 11, 2008. Also in 2008, Aycox starred in Joy Ride 2: Dead Ahead, the sequel to 2001's Joy Ride.

In 2006, Aycox guest starred in Criminal Minds, as Amber Canardo, a sociopathic serial killer, in the episode "The Perfect Storm." Also that year, she portrayed Meg Masters, a recurring antagonist, in the first season of the WB (now CW) series Supernatural. Executive producer Kim Manners had previously worked with Aycox in an episode of Over There that he directed, and hand-selected her for the role of Meg.

In 2003, Aycox played Minxie Hayes, a psychic cheerleader, in Jeepers Creepers 2. It was the sequel to the 2001 horror film Jeepers Creepers. From July to October 2005, Aycox portrayed Private Brenda "Mrs. B" Mitchell on Over There. The series followed a unit of the United States Army's Third Infantry Division on its first tour of duty in Iraq, and chronicled the war's effects on the soldiers' families in the United States.

Nicki Lynn Aycox (born May 26, 1975) is an American actress and musician, known for her roles in Supernatural, Jeepers Creepers 2, Perfect Stranger and The X-Files: I Want to Believe. She released her debut EP, Red Velvet Room, in 2015.