Values dropped 0.1 per cent from May, making them 0.9 per cent lower quarter on quarter.
However, prices are still 2.5 per cent higher than the same period last year.
The average home value stands at £237,616, according to the lender.
Despite the reduction in prices, mortgage activity was strong in June.
New enquiries were up by 100 per cent compared to May, while buyers also resumed purchases previously put on hold.
Russell Galley, managing director of Halifax, said: “The near-term outlook points to a continuation of the recent modest downward trend in prices through the third quarter of the year, with sentiment indicators, based on surveys of both agents and households, currently at or around multi-year lows.
“Of course, come the autumn, the macroeconomic landscape in the UK should be clearer and the scale of the impact of the pandemic on the labour market more apparent.
“We do expect greater downward pressure on prices in the medium-term, the extent of which will depend on the success of government support measures and the speed at which the economy can recover.”
David Westgate, group chief executive at Andrews Property Group, added: “Nobody can deny the property market is facing a huge amount of uncertainty given rising unemployment, but for now it is proving far more resilient than many expected.
“In some areas, we are actually seeing prices nudge up slightly as demand outstrips supply.
“Since mid-May, the pent-up demand that accumulated during lockdown has been unleashed on the market and has even put a slight spring in its step.
“We have just had the best four weeks of business trading in 2020 and the figures coming in are actually slightly higher than this time last year.
“The great unknown is whether the bounce we have seen in recent weeks is simply a dead cat bounce.”