If girls did not socialise with boys at school, "what happens when they go out into the workplace?", asked Richard Cairns, head of Brighton College.
Single-sex schools were a "deeply unrealistic world", said Mr Cairns, writing in a magazine.
But the Girls' Schools Association described his views as "old fashioned".
Writing in Independent School Parent, Mr Cairns complained too many parents were "swayed by outdated notions about girls performing better in single-sex schools".
Supporters of girls-only schools often argue pupils achieve better grades and are more likely to take subjects that are often male-dominated, such as maths.
'Non-plussed'
But Mr Cairns said female pupils at Brighton College, a co-educational private school, were "non-plussed when they read press reports about their supposed inability to thrive because they are sitting next to boys in class".
He said every year dozens of his female pupils achieved top grades in male-dominated subjects such as physics and went on to study sciences and maths at Oxford or Cambridge.
By contrast, women from all-girls' schools "may have a clutch of A*s and a first-class degree, but if they cannot meaningfully converse and communicate with male colleagues, they will be at a huge disadvantage", he warned.
"There is something, I feel, much more common to schools that educated both boys and girls, and that something is kindness," he added.
"Boys in single-sex school tend to create their own artificial hierarchies where only those in the first-15 rugby team are truly valued, while girls-only schools sometimes suffer a degree of emotional intensity that can lead to bullying.
"Contrast that with a co-educational world where girls admire the boys who dance, sing or act, and so, therefore, do the boys. Contrast that too with a mixed environment where the emotional intensity of all girls is diluted by the boys.
"In other words, there is a place for everyone and an environment where girls and boys can be themselves."
'Tiresome'
But Caroline Jordan, president of the Girls' Schools Association, said Mr Cairns might find the truth "unpalatable".
"Girls' schools feature heavily at the top of the league tables for independent schools and have done for decades," she said.
"It may also have escaped his attention that all-girls schools provide plenty of appropriate opportunities for interaction with boys; in fact, it is rather old-fashioned to assume anything other."
Ms Jordan also highlighted recent Institute of Physics research that indicated girls in single-sex private schools were more likely to study A-level physics than girls in mixed private schools.
"It is time for Mr Cairns to cease his rather tiresome attacks on independent-schools colleagues," she said.
"The sector benefits from diversity and choice, and I am sure he would agree with that."
