Jennifer was born in Kentucky. Her mother is Catherine Mitchell and her father is Robert Carpenter.

She attended St. Raphael the Archangel and then Sacred Heart Academy. During her last two years of high school, she studied drama at the Walden Theatre in Louisville, Kentucky. She then trained at the Juilliard School in New York City. In 2002, before she graduated, she made her Broadway debut in the revival of Arthur Miller's "The Crucible", starring Liam Neeson and Laura Linney.

Her breakthrough film role was "Emily Rose" in The Exorcism of Emily Rose (2005). She won a MTV Movie Award for "Best Frightened Performance" and a Hollywood Life Breakthrough Award. She was also named "Breakout Performer" at the 2006 Scream Awards.

In 2006, she cast as Dexter's adoptive sister in Showtime's Dexter (2006). Here, she met her first husband, Michael C. Hall.

In 2011, she starred in the off-Broadway play, "Gruesome Playground Injuries", at Second Stage Theatre and had a guest appearance on the CBS drama, The Good Wife (2009).

In January, 2014, it was announced that Carpenter will star in a new ABC drama Sea of Fire (2014), playing "FBI Agent Leah Pierce". However, the show was not picked into series.

In August, 2014, it was announced that she will provide the voice of "Juli Kidman" in the survival horror video game, PsychoBreak (2014), marking her first video game appearance. The game was released in October 2014.