Quilter was the deputy commissioner at the State Services Commission from 2007 to 2012, where she was responsible for the first five-year strategic plan for the Ministry of Social Development.[1] She worked on improving systems for governance and risk assessments, and led the implementation of the Defence White Paper 2010.[1][2]
Quilter served as the secretary of defence and chief executive of the Ministry of Defence from 2012 to 2019. Whilst in office, she led a reform of the defence capability management system.[1][3] She was reappointed as deputy public service commissioner, a position she retired from in 2023 after a 45-year career.[3]
Quilter was described as "a driver of modernisation and diversity while at the centre of some of New Zealand’s core public service organisations". In her Public Service Commission role she was responsible for achieving greater diversity and a 50/50 gender split for a group of thirty chief executives.[2] She also conducted a review into the workplace culture at Fire and Emergency New Zealand, and supported the public service commissioner through the COVID-19 response. Quilter cites Dame Margaret Bazley as her role model.[2]
Quilter has led and served on a number of boards, including the New Zealand School of Dance.[2] In the 1990s, after running out of space at home, she established a significant modern art collection, the Quilter Collection, which was on display for fifteen years at the Govett-Brewster Gallery.[2] The collection included works by Bill Hammond, Seraphine Pick and Tony de Lautour, among others.[4] Although she retained 30 works from the collection, Quilter later auctioned 47 others in order to fund an interest in 17th- and 18th-century religious art, and New Zealand artist Louise Greig.[4]