Coakley has taught at Lancaster University (1976–1991), Oriel College, Oxford (1991–1993) and Harvard University in the divinity school (1993–2007; as Mallinckrodt Professor of Divinity, 1995–2007). She was a visiting professor of religion at Princeton University (2003–2004). In 2006, she was elected the Norris–Hulse Professor of Divinity at the University of Cambridge (the first woman appointed to this chair) and took up the position in 2007. In 2011, she became deputy chair of the School of Arts and Humanities with a four-year appointment on the general board of the university. She stepped down as Norris–Hulse Professor in 2018 and was made professor emeritus. She has been an honorary professor of the University of St Andrews since 2018 and a visiting professorial fellow at the Australian Catholic University since 2019.