Ashley Bouder was born in Carlisle, Pennsylvania, and began her ballet training at the age of six with Marcia Dale Weary at the Central Pennsylvania Youth Ballet.

After attending the 1999 Summer Program at the School of American Ballet (SAB), the official school of New York City Ballet, she was invited by SAB to continue her training during the Winter Session. As a student, Ms. Bouder performed featured roles in George Balanchine's Dances Concertantes and Stars and Stripes for the School of American Ballet's 2000 Annual Spring Workshop. Bouder was named an apprentice with New York City Ballet in June 2000 and became a member of the corps de ballet that October. She was promoted to the rank of soloist in February 2004 and, in January 2005, was promoted to principal dancer.

As a principal in NYCB, she has won critical acclaim for her dancing in many Balanchine works, such as The Firebird, Stars and Stripes, and Emeralds and Rubies from Jewels, and Jerome Robbins works, such as Fall from The Four Seasons and Other Dances. Bouder has also originated roles for choreographers such as Peter Martins, Christopher Wheeldon, Wayne McGregor, Mauro Bigonzetti, Douglas Lee, Justin Peck, Liam Scarlett and Richard Tanner.

Her guest appearances include the Paris Opera Ballet, Rome Opera Ballet, the Mariinsky Theater, Teatro Massimo and Singapore Dance Theater. In addition she has participated in many ballet star galas worldwide.

She was the 2000 recipient of the Mae L. Wien Award for Outstanding Promise from the School of American Ballet and, in 2011 and 2013, respectively, received the Dance Open Awards for Expressivity and Virtuosity.