The multi-figured portrait of Murray will be on display in the London museum until May 3, after which time it will travel to the Scottish National Portrait Gallery in Edinburgh.
The painting will be exhibited in the National Portrait Gallery alongside four charcoal preparatory drawings of the Olympian and Wimbledon Champion.
"Andy Murray" came to life this past September, when Murray's newfound interest in art led him to meet and later sit for Hambling in her Suffolk studio .
"I'm quite naive when it comes to art so when I spend time with Maggi [Hambling] I tend to ask lots of questions and understand it better," the 32-year-old sportsman told the Guardian, adding that sitting for Hambling was a physical experience.
"I kind of thought I would basically just be sitting. Posing in these positions ... felt like quite a long time for me. I was there for three to four hours in total, we did have breaks. It was difficult, it was a physical morning," he continued, with Hambling conceding that she made him "do these impossible poses."
"If you think about tennis you're either hitting the ball against the sky or against the grass so Andy's movement between the two is very much what the painting is about .... Andy is about playing tennis. You are the most miraculous tennis player, that's why it had to work as a painting about movement," she told the British newspaper.
This is not the first portrait of Murray to enter the collection of the National Portrait Gallery, which also features a 2006 photograph of the tennis player.
Although best known for the public sculpture "A Conversation with Oscar Wilde," Hambling is also well represented in the London museum, where her portraits of actor Stephen Fry and Nobel Prize-winning chemist Dorothy Hodgkin are on display.