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Ayer was originally inhabited by the Nashaway, a Nipmuc people that inhabited the lands along the Nashua River and its tributaries. A small settlement was located along the banks of the Nonacoicus Brook, located in the western part of the town. The name of the Nashaway village, its people and the brook, pronounced by locals as /ˈnɒ nə ˌkɔɪ ʃəs/, was also recorded in early English sources as ‘Nonajcoyjicus,’ ‘Nonocoyecos,’ ‘Nonacoiacus’ and ‘Nonaicoics.’ According to the personal manuscripts of Justice Samuel Sewall, best known for his controversial role in the Salem witch trials, he was told sometime in 1698 by Hanah, wife of Sachem Ahaton of the Ponkapoag Massachusett tribe, that the name was actually Nunnacoquis (modern Wôpanâak Massachusett dialect Nunahkuqees /nənahkəkʷiːs/) and signified ‘an Indian earthen pot’ although literally refers to a ‘small dry earthen pot.’ The name was likely a reference to a series of small mounds along the banks of the Nonacoicus Brook.

Very little archaeological evidence has been found of settlement in the region, most likely lost to centuries of cultivation and development, although a handful of stone tools or evidence of habitation have been found along the shores of the Nashua River, Nonacoicus Brook, Sandy Pond and Long Pond as well as a rock shelter on Snake Hill. Although some have been dated to the Early Woodland Period (3000-2000 BP), the majority of findings are from the Late Woodland and Early Contact Period (1000-450 BP). In addition, portions of Main Street and Sandy Pond Road are believed to follow the vast network of trails used by Native peoples for trade, travel and communication. The Nashaway likely cultivated corn, beans and squash, but depended on foraging for fruits, nuts, tubers and seeds to supplement their diets. Seasonally, camps were set up in hunting areas, but the most important gatherings were likely the annual spawning migrations of Atlantic salmon, alewife, American shad, blueback herring and sea lamprey that once swam up the Nashua River from the sea via the Merrimack River.

The arrival of English settlers in the seventeenth century was a great disruption. Virgin soil epidemics such as smallpox, leptospirosis, influenza, scarlet fever and measles ravaged Native communities due to their lack of immunity to Old World diseases. The influx of English settlers also led to competition for land and resources and efforts to subjugate and assimilate the Native peoples. The Nashaway were visited by the missionary John Eliot, who had translated the Bible into the Massachusett language, understood throughout New England as a second language. He began teaching Indians to read and write, and to train as missionaries and teachers. Land was set aside for the Indians for the Praying town of Nashoba in what is now neighboring Littleton, Massachusetts, which likely attracted many of the Nashaway families in the surrounding areas. Nashoba was one of fourteen communities in the colony established for the Indian converts, where they came to meld English and traditional ways.