Hunt was educated at Christ the King Primary School, Cardiff, New College, Cardiff and King Edward VI Camp Hill School for Girls, Birmingham, before going on to study English Language and Literature at St Hilda's College, Oxford.
Hunt joined the Equality Challenge Unit in January 2004 where she led work to advise Higher Education Institutions on sexual orientation and gender identity equality.
In 2005, she joined Stonewall in the role of Senior Policy Officer where she led work on Stonewall's research into homophobic bullying in schools. She became Head of Policy and Research in 2007 and Director of Public Affairs in 2009.
During this time Hunt produced research into lesbian, gay and bisexual health needs and inequalities, religion and belief and its impact on sexual orientation equality, older gay people's experiences in Britain and, in 2012, the first guide looking at openly-gay role models.
In 2013, Ruth Hunt was named as Deputy Chief Executive of Stonewall, overseeing the strategic development and delivery of Stonewall's policy, research, campaigns and information functions which includes the work of Stonewall's Public Affairs team, Education team, the Stonewall Information Service and Stonewall Scotland and Stonewall Cymru.
In July 2014, after a period as Acting Chief Executive, she was named Chief Executive of Stonewall. Since taking on the leadership, Hunt has committed to bringing Stonewall even deeper into communities, engaging with groups from different ethnicities, religions and geographies – both in the UK and abroad.
She has also spearheaded Stonewall's commitment to campaign for trans equality, which will inform much of the charity's work going forward. This move followed an extensive consultation with over 700 trans people and will see the organisation campaign for legal and social equality for trans people.
Hunt has overseen the growth of Stonewall's work in Scotland and Wales, in particular the establishment of the Stonewall Cymru bilingual information service and Stonewall Scotland's lobbying to secure the Marriage and Civil Partnership (Scotland) Bill. She gave evidence to the Scottish Parliament Equal Opportunities Committee on marriage equality in September 2013.
Hunt leads Stonewall's work on policy development and strategic influencing, in particular developing strategic partnerships with organisations across the public and private sector. She has led work with organisations such as the Ministry of Defence, the UK Border Agency, the Home Office and Accenture.
As Deputy Chief Executive, Hunt was involved in Stonewall's campaign regarding the Marriage (Same Sex Couples) Bill in England and Wales.
She was involved in Stonewall's campaign regarding the Human Fertilisation and Embryology Act 2008, legalising lesbian to access fertility treatment.
In October 2013, in its "Pink List", the Independent on Sunday named Hunt as the fifth most influential LGBT person in Britain. In 2014 she dropped to eighth place in the renamed "Rainbow List", and in 2015 she was voted into third place. In 2015 she also received an honorary fellowship from Cardiff University and an honorary degree from Keele University.
She attracted much attention in May 2014 when she announced in the (UK) Daily Telegraph that Stonewall would not be joining a wide boycott of the Dorchester Hotel in London, owned by the Sultan of Brunei, where Stonewall was to hold a gala dinner. The Sultan was proposing to introduce the death penalty for sodomy but she argued that there was not "a mandate for the boycott" and "We only implement actions that we can calculate will have an impact."
She publicly apologised days before the May 2015 UK general election after Stonewall was criticised for publishing an online campaign graphic which suggested that only the Labour Party substantially supported LGBT equality in its manifesto. Lib Dem Minister Stephen Williams had told PinkNews: "I'm astounded by this grossly misleading graphic."
Hunt is a practicing Roman Catholic and has spoken out in favour of bridging the gap between faith leaders and LGBT communities.