Countrywide sold a 2.2% stake at the time of Zoopla's stock market flotation in 2014, before selling around half of its remaining 4.1% shareholding for £19.1 million in February.
Countrywide confirmed that it has sold in aggregate 9,234,473 ordinary shares in Zoopla at an average price of £3.17 between the period from 9th August 2016 to 21 September 2016.
It said the proceeds of the disposal will be used to "reduce corporate indebtedness and for other general corporate purposes".
Earlier this week, Zoopla announced a new partnership with online mortgage broker Trussle which will see visitors to Zoopla's website offered a Mortgage in Principle within five minutes.
Consumers can then arrange a viewing with a Mortgage in Principle in place, which Zoopla and Trussle say will "dramatically speed up the sales process".