Percy Johnson-Marshall took up his first university teaching position as Senior Lecturer in Planning at the University of Edinburgh's new Department of Architecture, in 1959. He taught Civic Design to architecture undergraduates and a postgraduate diploma course in Civic Design. In 1963 he began a course in Regional Planning and, the following year, became Professor of Urban Design and Regional Planning. Later he headed his own Department of Urban Design and Regional Planning, within Sir Robert Hogg Matthew's School of the Built Environment (1966-1967). Post-doctorial fellowships and postgraduate research were available within the Planning Research Unit (PRU), which Johnson-Marshall set up in 1959. The PRU, was independently funded and undertook research for a variety of governmental organisations including the Scottish Development Department. The Architecture Research Unit (ARU), formerly the Housing Research Unit, was set up by Sir Robert Hogg Matthew in 1959 and undertook research and design projects for various local authorities. There was also the opportunity for postgraduate research under its auspices. Johnson-Marshall deputised for Matthew as director of the ARU while the latter was engaged with duties for the Royal Institute for British Architects and International Union of Architects.

In 1985, the Patrick Geddes Centre for Planning Studies was opened under the directorship of Percy Johnson-Marshall. This was in the Outlook Tower, the symbolic headquarters of Sir Patrick Geddes, which the University of Edinburgh had acquired. He retired from the post in 1991.