Material from the prehistoric periods is presented in the first room, from the Stone Age (Paleolithic, Neolithic) and the Metal Ages (Copper Bronze, and Iron). Although several Paleolithic open-air sites are known from the Nin vicinity, none have been excavated to the present, so that only one stone point from the Mousterian Culture (100,000 – 35,000 BC) is exhibited from this period. On the southern edge of the present-day salt-flats, at the site of Koludrovicka, a settlement was formed in the Neolithic with characteristics of the Impresso Pottery Culture (5500 – 5000 BC). Stone tools and characteristic fragments of pottery vessels found at this site are displayed. The only finds from Nin known to date from the Copper Age (or Eneolithic) were discovered at the position of the later forum, and they consist of fragments of pottery decorated with wart-like protrusions, zig-zag patterns, stamped triangles, and so forth. The fragments are dated to the late Copper Age (2500 – 2000 BC). The Nin area contains a series of stone and earthen mounds with remains from the Bronze Age (2000 - 900 BC). So far 136 grave mounds have been registered in the area of the present tourist settlement of Zaton, only some of which have been excavated. The cultural remains discovered include pottery fragments, jewellery, tools, weapons, various shells, and animal bones. A bronze dagger from this site is featured in the exhibit case, along with a stone mould for casting axes, a fragment of a bronze axe, and spears from Nin. A settlement of the tribe of the Liburnians was formed on the small island that is Nin at the very beginning of the Iron Age (ca. 900 BC). The numerous finds of pottery (various forms of bowls, weights, spindle-whorls, baking lids, platters, etc.) discovered around the Church of the Holy Cross and St. Anselm, as well as at the site of the Roman temple, all offer evidence of the culture, the lifestyle, and their development. The rich grave finds dated to the period from the 9th to the 1st centuries BC particularly stand out (jewellery: earrings, rings, brooches (fibulae), combs, pins; pottery from Italy: Apulian Geometric and Daunian). The burial customs of the Liburnians are illustrated by the reconstruction of a child's grave in an urn, and a deceased individual placed in a contracted position in a stone coffin formed of slabs. The independent development of the Liburnian Culture ceased with the Roman conquest of this region at the end of the 1st century BC. 

Remains from the Roman period are presented in the second room (from the end of the 1st century BC to the 4th century AD). Aenona, or Roman Nin, received the status of a Roman municipium around 16 BC. The appearance of the city was considerably modified during the 1st century AD: walls were erected and a bridge, a gate with towers, and a water supply system were built, the streets were laid out in a regular pattern and paved, and finally a forum was constructed at the crossing of the main streets, with a magnificent temple dedicated to the Capitoline triad. On display in the museum is an imperial portrait head of the emperor Nerva (96 – 98 AD) that was discovered at the forum in 1989. The constantly increasing trade and transportation connections led to the importation of various goods dominated by objects of everyday use, made of pottery (dishes, bowls, cups, amphorae, pots, jugs, lamps), glass (flasks, balsamaria, drinking vessels), amber, metal (coins, earrings, brooches/fibulae, rings, buckles, chains, mirrors, tools), and bone (decorative pins, cosmetic equipment). The Roman government in Aenona introduced the religion of worshipping the Roman gods and imperial family, as is confirmed among other things by votive altars dedicated to Jupiter and Silvanus and a bust of Dionysus. The indigenous Liburnian gods that continued to be worshipped included Anzotika, the goddess of fertility.
    

The third room presents the Early Christian period (from the 4th to the early 7th cent.).
The most recent archaeological excavations have confirmed that the earliest Christian congregation met in a private home adjacent to the present-day parish complex. A longitudinal ecclesiastical structure was built in the 5th century above the house, and during the reign of the Byzantine emperor Justinian (527 - 565) a new and larger church was constructed. At the same time the basilica of the Virgin Mary was built, located on the northern side of the island, and the Church of St. Andrew in the Roman harbour in Zaton. Fragments of church furnishings are displayed along with fragments of pottery and glass vessels with characteristic forms and designs for this period. A separate case features the finds from grave 41 excavated at the position of Ploce in the parish complex. Two female individuals were buried in the grave with exceptionally valuable jewellery made of gold and silver (earrings, rings, torcs). The grave is dated to the 6th-7th centuries. 

The early medieval period (from the early 7th to the end of the 11th centuries) is presented in the fourth and sixth rooms. The fourth room displays early Croatian grave goods collected through many years of excavation both at cemeteries of the pagan horizon (from the early 7th to the middle of the 9th century): Materiza, Ždrijac, and Banovac, and also at cemeteries with Christian features (from the mid-9th century to the end of the 11th century): by the Church of the Holy Cross and St. Anselm's. The pagan stratum is represented by finds of pottery vessels, knives, razors, awls, buckles, and so forth, while the Christian stratum is represented by jewellery finds (earrings, rings, buttons).  Grave 322 from the cemetery at Ždrijac is displayed in a separate case. This was the grave of the family of a Croatian dignitary (a man, woman, and child) where 38 different items were found, among which the warrior equipment stood out (a sword, a spear, spurs). The sixth room deals with the theme of ecclesiastic architecture. The room is dominated by the copy of the baptismal font from the period of Prince Višeslav dated to beginning of the 9th century. The font is one of the most important monuments of the early medieval Croatian state. Along with the font, numerous stone fragments are displayed of church fittings decorated with interlaced designs discovered during excavation in the churches of St. Anselm, the Holy Cross, and the Virgin Mary. A copy is also displayed of the stone beam (architrave) of the altar screen discovered during demolition of the Church of St. Michael in 1911. The name of Prince Branimir (879-892) is cited on the beam, along with the titles dominus and dux sclauorum.
    

A special pavilion was built (room 5) to display the results of the many years of underwater excavations in the region of Nin and at Zaton, where the Roman harbour of Aenona was located. The room is dominated by the two early Croatian ships (Condura Croatica) discovered at the entrance to the Nin harbour. The larger boat was conserved and entirely reconstructed, while the other was conserved and presented in the condition in which it was preserved. Radiocarbon analysis (C14) of wood samples has dated the boats to the second half of the 11th century. A partly reconstructed serilia, the vessel used by the prehistoric Liburni and Histri, is also displayed with these boats. The name serilia indicated that they were "sewn" or held together by ligatures in the form of linen and broom cords. The remains of three Liburnian seriliae have been discovered to date in the Roman harbour at Zaton. The last case displays numerous remains of ship equipment, fishing tackle, pottery and glass vessels, coins, jewellery, and other material that was discarded or fell by chance into the silty bottom of the Roman harbour at Zaton. 
    

The seventh room displays items related to the Middle Ages and Early Modern Period (from the beginning of the 12th century to the 28th of April 1646, when Nin was destroyed to its very foundations by "friendly" cannon fire from Venetian battleships for strategic reasons involving the fear of its capture by the Turks). The archaeological material is displayed in two cases. The small case exhibits a large quantity of pottery material found in the cultural layers surrounding the churches of the Holy Cross and St. Anselm, belonging chronologically to the period from the beginning of the 12th century to the end of the 15th century. The most common jewellery items were earrings (three-jointed earrings and three-beaded earrings), rings, and buttons found in the graves around the churches of St. Anselm and St. Ambrose. A larger case displays objects from the Prefect's Palace, one of the most important medieval public structures in Nin. Excavations within the building encompassed parts of two buildings and a refuse pit. The cultural layers of the refuse pit contained around 3500 fragments of pottery and glass material, metal objects. shells, and animal bones. The discovered pottery and glass material deposited in the refuse pit chronologically documents life in the palace from the very beginning of the 15th century to the middle of the 17th century.      

The stone monuments from Nin and its immediate surroundings are on display in the lapidarium. The collection consists of stone monuments from the Roman, Medieval, and early Modern periods. These monuments were mostly gathered at the beginning of the 20th century, when they were placed in the Antiquity Collection in and around the Church of the Holy Cross. When the collection was moved to its new location, some of the monuments were utilized for the permanent exhibition of material from the Roman and Early Croatian periods, while the others were placed in the courtyard. The collection of stone monuments has increased considerably in the past ten years as a result of the numerous archaeological excavations and conservation projects in Nin and the vicinity.