Average asking prices rose by 0.7% to £267,440 over the month to September, marking the first increase since May.
Rightmove says its index could be an early sign of an autumn bounce, as the increase is higher than the 0.5% monthly rise last September.
However, it warns that there is “considerable ground to make up” after a subdued summer.
Sellers are facing a “crowded market” as the number of homes listed for sale is at a 12-year high.
But the number of newly-listed properties is 3% lower than last September, indicating that homes are lingering on the market for longer.
Despite the post-summer holiday rebound in buyer activity, the number of enquiries are 9% lower than this time last year.
The number of sales agreed is also 9% lower than last year.
Rightmove property expert Colleen Babcock says: “September’s above-average price rise is a welcome sign of confidence after a particularly subdued summer, but it should be viewed as a modest recovery rather than a major turning point.
“Property prices have largely underperformed against the long-term average this year, but September is an exception.
“While buyers and sellers are returning to the market after the summer holidays to potentially fuel an autumn bounce, sellers face stiff competition.
“With a large crowd of sellers chasing a smaller number of buyers, realism on pricing or a high-quality finish are absolutely key to attracting a buyer and making a sale.”
Together chief commercial officer Ryan Etchells says: “In defiance of the recent gloom which has beset the property market, a monthly growth in house prices according to Rightmove shows us that the market may be more resilient than previously thought.
“But despite some encouraging signs in the data, the increase may well be the final ray of light before a difficult winter for the market.
“Although the Bank of England kept interest rates at 3.75% last week, the chances of multiple rate-hikes in the next few months remains high.
“If this proves to be the case, we need to prepare for falls in house prices in the near term.”
North London estate agent and former Royal Institution of Chartered Surveyors residential chairman Jeremy Leaf says: “After a quiet few months, the increase in viewings since the end of the summer holidays has meant sellers are more optimistic about their prospects of finding a buyer.
“However, asking prices are not selling prices.
“Rather, they are an aspirational starting point, which determines whether any interest is generated in a property.
“In our offices, affordability concerns remain, prompted by rising inflation and mortgage rates, as well as fear as to what might be in store in next month’s budget.
“We are finding that only those sellers who understand the need for flexibility are receiving acceptable offers.
“Even then, the pace of sales is painfully slow bearing in mind the ample choice of property in most price ranges.”