Attendees audibly gasped as fierce bidding pushed prices far beyond expectations at Dreweatts.
A self-portrait by Ms Richardson, who famously established child art as a vehicle for self-expression, sold for £6,930, dwarfing its estimated £300-£500.
The lot also included works given to Ms Richardson by renowned artist and critic Roger Fry.
These included the earth-toned painting Wooded Landscape with Hills Beyond, which came with a Christmas dedication to Ms Richardson from Mr Fry and sold for £8,820, against an estimate of £700-£1,000.
A colourful Mr Fry still life, titled Still Life of a Jar, Apples and a Candlestick Holder, realised the same price.
His works were personally gifted to Ms Richardson and came directly from the artist.
Further pieces from the British School and esteemed artist Graham Sutherland were included in the collection.
Mr Sutherland’s etching Pastoral, dated 1938, bolted to an impressive £15,120, against an estimate of £800-£1,200.
Francesca Whitham, picture specialist at Dreweatts, said, “We are thrilled with the result of this wonderful group of works from the collection of Marion Richardson.
“The fact that it made over four times its pre-sale estimate, shows the demand for fresh to the market works with an interesting provenance and the continued popularity of works connected to the Bloomsbury School artists.”
Ms Richardson’s ground-breaking practices, which encouraged children to articulate their individuality and emotions through art, established her as a game changer in art education.
Her influence cemented her legacy, and a London primary school even carries her name today.
This auction marked the first time Ms Richardson’s personal art collection, which remained in her family for many years, has been offered on the market.