After a brief spell at Derby County in 1986, he joined Shrewsbury Town for a £30,000 fee. In two years with the Shrews, Linighan made 65 league appearances, scoring one goal.[3]
Linighan joined Ipswich Town in 1988 for £300,000.[5] In eight years, he made a career-high 277 league appearances, scoring twelve goals, and played in the Premier League for three seasons (1992 to 1995).[5]
Scottish club Dunfermline Athletic came in for the defender's services in 1998,[3] and he moved north of the border for what proved to be just one game. During his time with the Pars, he was loaned to Mansfield Town, whom he would join on a permanent basis in 1999.[3]
In 2000, Linighan moved into non-league football with Southport and Chester City,[3] before a short spell with Hyde United in 2002 where he made eleven appearances,[6] before retiring.[5]