A new display about Dorothée Pullinger unveiled today includes the Galloway coupe which she helped market to female drivers in the 1920s.
French-born Pullinger, known as Dolly, was also an accomplished racing driver.
She was also the first woman in the Scottish Engineering Hall of Fame.
The exhibition also helps mark the centenary of the Women’s Engineering Society (WES), which she co-founded in June 1919.
Pullinger managed the factory at Heathhall, near Dumfries, which launched the museum's car in 1924.
She challenged gender bias after her application to join the Institution of Automobile Engineers in 1914 was rejected by being told "the word 'person' means a man and not a woman".
Engineering historian Dr Nina Baker said she hoped the showcase for Pullinger would help female engineers "put across their stories better".
She told The Scotsman: "It is not just about history. It will help today's young women and engineers understand they are not making unusual career choices.
"For Dorothée Pullinger to be told it was unusual was a fact, but to say that now would be outrageous.
"There are TV soap operas featuring scientists and doctors, but none about engineers - people do not know what an engineer does all day."
Transport and technology curator Neil Johnson-Symington said: "She had a real flair for engineering.
"I would like to think she was involved in every element of the car production, leading the workers and the assembly."
David McDonald, who chairs Glasgow Life, which runs the museum for Glasgow City Council, said: "We hope this new display will assist in ensuring her story continues to inspire others, particularly girls, to live as she did and follow their dream of becoming an engineer."
She was born in 1894, the daughter of car designer Thomas Pullinger.
The family moved to the UK and in 1910 she started work at car manufacturer Arrol-Johnston in Paisley, where her father was a manager.
She was awarded the MBE for running a munitions factory at Barrow-in-Furness in Cumbria during the First World War, which employed some 7,000 women.
She went on to manage the Galloway Engineering Company, a subsidiary of Arrol-Johnston, which produced the coupe.
Smaller and lighter than most cars of the time, it featured gears in the middle of the car rather than outside, the steering wheel was smaller, with the seat raised and the dashboard lowered.
The Riverside's model is one of only around 15 remaining of the 4,000 made.
Dorothée Pullinger's daughter Yvette Le Couvey, 93, said she had become an engineer simply because she wanted to follow her father's career.
She recalled her mother still behind the wheel into her late 80s
She said: "She enjoyed driving. There was no messing about - she knew how a car worked, and if something was wrong, she would fix it.
"She was certainly a trailblazer for women - it's just a pity she could not be recognised more in her time.
"I hope the exhibition will make women realise they can do this - this is an opening for them."
Pullinger's racing career included being the first woman to enter the Scottish Six Days Reliability Trials in 1924, in which she won the silver cup.
She also won a medal from the Edinburgh and District Motor Car Club in 1922.