He was selected without any great controversy as the first Chief Architect of the Metropolitan Board of Works on 1 February 1856. Marrable was not a particularly well-regarded architect but no greater figure applied for the job, partially because the salary being offered was relatively low, but also because the architect would largely be responsible for building roads and not distinctive buildings. Marrable approached this task with a methodical eye, but often ended up being perceived as boring, as The Elector for 27 June 1857 said that he was "squeezing every word to death almost in a half-closed mouth, so that nobody scarcely knows what he says".
Under his supervision, Garrick Street and Southwark Street were designed. When the Metropolitan Board obtained a site at Spring Gardens to build its headquarters, Marrable was naturally engaged to design it. He produced a three-storey building in the Italianate style, which (after subsequent enlargements) was impressive for Nikolaus Pevsner to regard as the chief interest in the street.
After his resignation, Marrable designed his most notable surviving building, the Garrick Club (1864) which was again in an Italianate palazzo style. The Garrick is fronted in Portland render which blackened over the years; proposals to clean it did not receive the support of club members until 2005. Marrable married Madeline Cockburn, a painter, in the same year. He continued to work occasionally on Metropolitan Board of Works compensation matters; an inquiry many years after his death found evidence that he may have been corrupt. Another building designed by Marrable was St Peter's Church in Deptford (1866-70).