The average price tag on a home fell by £3,600 in August as "Brexit uncertainty" combined with the summer holiday slowdown.
The £3,602 month-on-month fall in the price of property coming to market took the average asking price across England and Wales to £304,222 in August, property website Rightmove said.
Despite the decrease, the average asking price is still 4.1% higher than it was a year ago.
Rightmove said the 1.2% month-on-month fall in asking prices is in line with average decreases usually seen during the summer holidays.
But it predicted 2016 will be a "year of two halves" for the housing market, with a surge in buyers already having been seen in the first half of the year as buy-to-let investors rushed to beat a stamp duty hike which was imposed for this sector on April 1. Many purchases were brought forward which might otherwise have taken place later in the year.
Miles Shipside, director at Rightmove, said: "Many prospective buyers take a summer break from home-hunting, and those who come to market at this quieter time of year tend to price more aggressively.
"This summer is also affected by both Brexit uncertainty and the aftermath of the buy-to-let rush in March to beat the stamp duty deadline."
Larger family-sized homes with four bedrooms or more would benefit the most from any autumn pick-up in activity, Rightmove said. These properties are taking an average of 74 days to sell, while smaller homes favoured by first-time buyers and people taking their second step on the property ladder are typically taking just 58 days to be snapped up.
The figures also show that despite the monthly price dip, the North East of England is the only region where asking prices are lower in August than a year earlier. The average asking price in the North East is £147,330 - 1.2% down on August 2015.
The East of England has seen the biggest percentage hike in asking prices over the last year, with the average asking price there at £334,951 - 8.2% higher than in August 2015.
In London, asking prices fell by 2.6% in August - the biggest month-on-month dip of all the regions. The average asking price in London is £619,409, which is still 2.1% higher than a year ago.
In Wales, asking prices edged down by 0.2% month-on-month to reach £180,425 on average.
Yorkshire and Humber and the West Midlands were the only regions to buck the trend of a month-on-month asking price fall, with asking prices in these regions increasing by 1.2% and 1.1% respectively.
Rightmove said the southern regions, which tend to be influenced by the London market, have seen bigger jumps in the length of time it takes to sell a property than northern regions over the last couple of months.
The time it takes to sell a home in London increased by five days between May and July, while in the South East and the South West the length of time to sell increased by four days and in the East of England the length of time increased by three days.
While the average number of days it takes to sell a property is still generally longer in the North than in the South, all of the northern regions have seen either no change in the average length of time to sell or just a day plus or minus over the same period.
Mr Shipside said: "It will be welcome news for some northerners that the traditional North-South divide may be taking a rare turn in their favour."
He continued: "At this time of year, interest from buyers of more expensive properties that typify much of London and its commuter belt tends to tail off more, as they are often discretionary movers.
"Having waited for the referendum result, it now seems that some are also waiting until the summer holidays are over before reviewing their course of action."