She was born in Dublin, Ireland, to the Irish actor/director Shelah Richards and the playwright Denis Johnston, a cousin of the late actress Geraldine Fitzgerald, via Fitzgerald's mother, Edith. She was educated at Trinity College Dublin, and currently lives in Derry, Northern Ireland. She was born into the Church of Ireland and many of her novels deal with the fading of the Protestant Anglo-Irish ascendancy in the 20th century.

She is a member of Aosdána.

Novels

• The Captains and the Kings (1972) winner of the Author's Club First Novel Award
• The Gates (1973)
• How Many Miles to Babylon? (1974)
• Shadows on Our Skin (1977) shortlisted for the Booker Prize
• The Old Jest (1979), winner of a Whitbread Book Award for 1979
• The Christmas Tree (1981)
• The Railway Station Man (1985)
• Fool's Sanctuary (1988)
• The Invisible Worm (1992)
• The Illusionist (1995)
• Finbar's Hotel, edited by Dermot Bolger (1997) (Contributor)
• Two Moons (1998)
• The Essential Jennifer Johnston (1999) (contains The Captains and the Kings, The Railway Station Man, and Fool's Sanctuary)
• Great Irish Stories of Murder and Mystery (2000) (Contributor)
• The Gingerbread Woman (2000)
• This is not a Novel (2002)
• Grace and Truth (2005)
• Foolish Mortals (2007)

Plays

• The Nightingale and Not the Lark (1981)
• Indian Summer (1983)
• Andante un Poco Mosso, in The Best Short Plays 1983, (1983)
• The Porch (1986)
• A Play in Two Acts (1996)