Ferriter is Ireland's best known historian and is Professor of Modern Irish History at University College Dublin, a position he was appointed to in 2008 at the age of 35. He was formerly a senior lecturer in history at St. Patrick's College, Drumcondra, Dublin City University. He was the host of What If, the popular Sunday morning radio programme that broadcast weekly on RTÉ 1 from 2003-2009, and also presented RTE's History Show from 2011-13. His 2004 book The Transformation of Ireland 1900–2000, at 900 pages and containing many new perspectives on modern Irish history, was considered a landmark publication. In 2007, Ferriter wrote the critically acclaimed biography, Judging Dev. This was an insight into one of Ireland's most influential leaders, Éamon de Valera. It won in three categories of the 2008 Irish Book Awards, an achievement that remains unmatched. He was Burns Scholar at Boston College from 2008 to 2009. His 2009 book Occasions of Sin: Sex and Society in modern Ireland is considered the definitive history of Irish sexuality in the twentieth century and was described by the Sunday Times as a "rigorous, empirical and layered examination of a topic that befuddled Irish people for most of the last century". In June 2010, he presented a three-part television seriesThe Limits of Liberty, about how the senior politicians of the Irish Republic and Irish Free State were more concerned about holding on to power than changing policy for the benefit of the people. He has collaborated closely with Emmy award-winning producer Nuala O'Connor; their 2018 film Keepers of the Flame deals with the legacy of the Irish revolutionary period of the early twentieth century. Ferriter's book, Ambiguous Republic: Ireland in the 1970s, published in November 2012, considers the widespread social, cultural, economic and political upheavals of the decade, a time when the Northern Irish Troubles profoundly affected the governance of the Republic, when Ireland joined the EEC, when for the first time a majority of the population lived in urban areas, and when economic challenges abounded. The 1970s in Ireland also witnessed an increasingly visible feminist movement, and the political and legal establishments and other powerful institutions including the Church began to be subjected to a new criticism. In 2013, Ferriter played a leading role in the Democracy Matters group that successfully campaigned against the government's proposal to abolish the Irish Senate; the proposal was defeated in a referendum in October 2013. In 2014 he became a weekly columnist with Ireland's leading quality broadsheet newspaper, The Irish Times. In 2015, Ferriter published his account of the revolutionary years of the early twentieth century in A Nation and Not a Rabble: The Irish Revolution 1913-1923. Based on new sources and perspectives, it was acclaimed by the Irish Independent as "magisterial", and "giving voice to history's silent souls". Ferriter's book The Irish Border: The Legacy of a Century of Anglo-Irish Politics was published in February 2019 to critical acclaim in both the UK and Ireland and became a bestseller. The Times hailed it as "a rare pleasure" suggesting that anyone who wanted to understand why Brexit was proving such an intractable difficulty needed to read this book; the Irish Independent described it as a "deft history of the problem child nobody wants" while it was hailed in The Irish Times as "invaluable". In March 2019, Ferriter was elected a member of the Royal Irish Academy.
