The school was founded by Alderman William Preston, one time Mayor of Liverpool, and the Vicar of St. Margaret's, Anfield, Reverend John Sheepshanks. The school opened in 1879 by the parish dignitary and MP for West Toxteth, Mr TB Royden. The school's first Headmaster was Mr E Crossley and an early teacher and benefactor was Mrs Gertrude Langton. Preston, Sheepshanks, Royden, Crossley and Langton are commemorated in the names of the current School Forms. In the 2015/2016 academic year, the form Walton was added in commemoration of the school's first female headteacher. The school began as a Higher Grade School and after the 1918 Education Act, St Margaret's was recognised as a Central School with a selective intake based on a competitive examination. After the Education Act 1944, the school was restyled St. Margaret's Church of England School and during the 1950s courses leading to the GCE 'O' Level and 'A' Level examinations were established. In 1963 the school moved from Anfield to Aigburth. In the 1970s it had around 550 boys. In 1980 it was enlarged to a four-form entry school for students from 11 to 18 years of age. This was the year that the school had their first intake of girl students. There were two other secondary schools in Liverpool also called St Margaret - St Margaret Mary's RC Secondary Modern School, a mixed school on Pilch Lane and St Margaret Cltherow RC Secondary School, a girls' school on Ullet Road. St Margaret's is a Church of England High School and was awarded Technology College status in 1997, and Specialist Language College status in 2008. The school increased its intake to five-form entry in September 1998. In September 2015 the school again increased its intake to six-form entry. It is now an Academy as of 2014.
New buildings
In recent years, three major building developments, the Technology Suite, Sixth Form Centre and the Humanities and Administration Suite, have considerably improved the school's teaching and administration facilities. The Cricket and Sports Centre opened in 2006. In 2010 the school were given funding on behalf of Building Schools for Future Program. Originally the school was going to move to a new site on Edge Lane; however, the Governors disagreed, and the school remained at Aigburth, but instead the school rebuilt the main office, and the main corridor was updated. In 2014, 6 more classrooms and a new examination hall have been built to replace old classrooms on the yard, taking the place of the old gymnasium. In 2016, new food technology and drama departments were built, as well as the renovation of the cafeteria.
Academic performance
In 2019, the school's Progress 8 measure for GCSE was average. Attainment 8 score was above average. The proportion of children achieving Maths and English GCSEs was considerably above average. The proportion of children entering the English Baccalaureate was considerably lower than average. The average A level grade was C+, in line with the England average, and the average A level points score was 32, below the England average of 24. Attainment 8 score was above average. As of 2020, the school's most recent inspection judgement from Ofsted was Good, in 2015, confirmed by a short inspection in 2018.