Phillips began her career as a Helena Rubinstein Fellow in the Whitney's Independent Study Program in 1976 and became a curator in 1982.

During her twenty-two-years at the Whitney, she organized over thirty exhibitions, including the notable thematic exhibitions "The Third Dimension: Sculpture of the New York School” (1984); “High Styles: the History of American Design” (1985); “Image World: Art and Media Culture” (1989); “Beat Culture and the New America, 1950–1965” (1994); and “The American Century Part II: 1950–2000” (1999); midcareer surveys of works by Terry Winters (1986), Cindy Sherman (1987), Julian Schnabel (1987), and Richard Prince (1992); as well as a major retrospective of the work of Frederick Kiesler (1988).

The presence of the museum on the Bowery also spurred a renaissance of the street and neighborhood, including a new district for galleries and creative spaces.

The New Museum created a dedicated space for digital art projects in 2000 (Media Z Lounge), which subsequently led to bringing on Rhizome as an affiliate organization in 2003.

[5] Phillips has served and continues to serve on several boards and advisory boards, including the Fabric Workshop and Museum, the Fulbright Fellowship Program, the Andy Warhol Foundation for the Visual Arts (for which she was a trustee and executive committee member from 2002 to 2012), White Columns, Lower Manhattan Cultural Council, the Azuero Earth Project, CIFO, the Frederick Kiesler Foundation, the Jay DeFeo Trust, and the Association of Art Museum Directors, where she is the chair of the Professional Issues Committee and works on the Futures Task Force.

In 2013, she helped lead a study of the gender-based compensation disparity among American museum directors, which received national attention.