This was followed by Danesborough and Walton (£375,000) and Loughton and Shenley (£365,000).
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By contrast, the cheapest areas of Milton Keynes to purchase property were Woughton and Fishermead, which had a median house price of £225,000, Bradwell (£257,500) and Wolverton (£263,000).
The median – the middle number in a series – is used to ensure the figures are not skewed by extreme highs or lows.
Meanwhile, the number of homes sold in Milton Keynes rose from 3,418 in 2020 to 4,099 last year.
Of sales last year, 9% (386) were in Danesborough and Walton – making it the busiest area for buyers.
At the other end of the scale, Woughton and Fishermead saw just 83 properties sold in 2021, earning it the title of quietest area of Milton Keynes' property market, along with its cheapest.
The Centre for Economics and Business Research said that following a period of significant growth during the pandemic, it expects house prices to experience downward pressure over the next year, as a result of sharp rises in mortgage rates.
Karl Thompson, an economist at the think tank, said the strongest price contractions are expected outside of London and the South East, causing greater regional price disparities.
Grainne Gilmore, head of research at Zoopla, said: "The demand for larger detached homes during the pandemic has pushed average values for houses higher over the last year, while price growth for flats has lagged.
The ONS figures also reveal the trendiest area – the one which saw the fastest growth in sales – in Milton Keynes.
Of the 17 wards with at least 100 properties sold, Bletchley Park saw 54% more properties sold in 2021 than in 2020, followed by Newport Pagnell South (51%) and Olney (46%).