After the dissolutionment of the monasteries, much of the land at Penmon came under the ownership of Sir Richard Bulkeley. It is believed that under his instruction the dovecot was built around 1600. With 1000 nesting boxes the dovecot was able to house domestic pigeons for their eggs and meat. A pillar in the centre gave access to the boxes via a revolving ladder and a domed roof with a small cupola allowed the birds to fly in and out.
