Jamie Brown, a newcomer to Milton in 1999, started the little book shop, John Milton and Company, which celebrated its opening on Valentine's Day of that year.  In December of 1999 he invited about ten poets to read together in his bookshop in celebration of the English poet John Milton, for whom the Town of Milton was named in 1807.  Most were colleagues and friends from the Washington DC poetry scene, with the exception of H. A. Maxson of Milford, Delaware, and Shelly Grabel of Milton.

The following year there were twenty people, twelve readers and guests, and in 2001, thirty five, sixteen of whom shared their poems. The third year was the first time Fleda Brown, then-newly-appointed Poet Laureate of the State of Delaware, joined to commemorate the Town's namesake. 

Year four saw the event move to the second floor of the Milton County Library, where participants and audience numbered over fifty-five.  At that event, Sam Calagione, Founder and CEO of Dogfish Head Craft Brewed Ales established the Dogfish Head Poetry Prize for a chapbook manuscript of poetry. 

The first Annual Dogfish Head Poetry Prize was awarded in year five, 2003, the first time the event was held in the historic Milton Theatre.  Even without heat in the building, this multi-day event was a huge success. Several hundred people came through the doors of the theatre, including students from the Mariner Middle School, who had researched the life of John Milton and written poetry about him. Local merchants contributed cash prizes to each of the winners. James Keegan, PhD, who teaches at the University of Delaware, won the first Dogfish Head Poetry Prize for his manuscript, Fathers and Sons. The Prize consists of $200.00 and two cases of Dogfish Head Craft Brewed Ales. Year five also saw Grace Cavalieri, the host of the public radio program, The Poet and the Poem, moderate panels on the importance of poetry to our understanding of history, culture, and politics.

Since 2003, the John Milton Celebration of Poets and Poetry has thrived, with the number of poets, festival-goers, participating schools and local sponsors continuing to grow. In 2005, Bay Oak Publishers of Milford and Dover, Delaware began to publish the Dogfish Head Chapbook series. Chapbooks published since the inaugural title are The Most Daring of Transplants (2004) by Emily Lloyd, Murmur (2005) by Michael Blaine, and Field Recordings (2006) by S. Scott Whitaker.
This year, a committee of poets from throughout the state of Delaware are organizing the event, with the Milton Schools night, Friday December 7th, coordinated by Joan Martin-Brown, of Milton.