diff --git a/src/nanoarrow/ipc/reader.c b/src/nanoarrow/ipc/reader.c
index d8d61f768..392aec832 100644
--- a/src/nanoarrow/ipc/reader.c
+++ b/src/nanoarrow/ipc/reader.c
@@ -28,6 +28,10 @@
 #define ENODATA 120
 #endif
 
+// Sentinel value to indicate that we haven't read a message yet
+// and don't know the number of header prefix bytes to expect.
+static const int32_t kExpectedHeaderPrefixSizeNotSet = -1;
+
 void ArrowIpcInputStreamMove(struct ArrowIpcInputStream* src,
                              struct ArrowIpcInputStream* dst) {
   memcpy(dst, src, sizeof(struct ArrowIpcInputStream));
@@ -186,6 +190,7 @@ struct ArrowIpcArrayStreamReaderPrivate {
   int64_t field_index;
   struct ArrowBuffer header;
   struct ArrowBuffer body;
+  int32_t expected_header_prefix_size;
   struct ArrowError error;
 };
 
@@ -230,7 +235,7 @@ static int ArrowIpcArrayStreamReaderNextHeader(
     // propagated higher (e.g., if the stream is empty and there's no schema message)
     ArrowErrorSet(&private_data->error, "No data available on stream");
     return ENODATA;
-  } else if (bytes_read == 4) {
+  } else if (private_data->expected_header_prefix_size == 4) {
     // Special case very, very old IPC streams that used 0x00000000 as the
     // end-of-stream indicator.
     uint32_t last_four_bytes = 0;
@@ -259,6 +264,14 @@ static int ArrowIpcArrayStreamReaderNextHeader(
   NANOARROW_RETURN_NOT_OK(ArrowIpcDecoderPeekHeader(
       &private_data->decoder, input_view, &prefix_size_bytes, &private_data->error));
 
+  if (private_data->expected_header_prefix_size != kExpectedHeaderPrefixSizeNotSet &&
+      prefix_size_bytes != private_data->expected_header_prefix_size) {
+    ArrowErrorSet(&private_data->error,
+                  "Expected prefix %d prefix header bytes but found %d",
+                  (int)private_data->expected_header_prefix_size, (int)prefix_size_bytes);
+    return EINVAL;
+  }
+
   // Legacy streams are missing the 0xFFFFFFFF at the start of the message. The
   // decoder can handle this; however, verification will fail because flatbuffers
   // must be 8-byte aligned. To handle this case, we prepend the continuation
@@ -300,6 +313,20 @@ static int ArrowIpcArrayStreamReaderNextHeader(
   NANOARROW_RETURN_NOT_OK(ArrowIpcDecoderVerifyHeader(&private_data->decoder, input_view,
                                                       &private_data->error));
 
+  // Set the expected number of prefix bytes for reading the next message
+  // if we haven't encountered a message yet.
+  if (private_data->expected_header_prefix_size != kExpectedHeaderPrefixSizeNotSet) {
+    switch (private_data->decoder.metadata_version) {
+      // Earlier versions raise an in header verification
+      case NANOARROW_IPC_METADATA_VERSION_V4:
+        private_data->expected_header_prefix_size = 4;
+        break;
+      default:
+        private_data->expected_header_prefix_size = 8;
+        break;
+    }
+  }
+
   // Don't decode the message if it's of the wrong type (because the error message
   // is better communicated by the caller)
   if (private_data->decoder.message_type != message_type) {
@@ -485,6 +512,7 @@ ArrowErrorCode ArrowIpcArrayStreamReaderInit(
   ArrowBufferInit(&private_data->body);
   private_data->out_schema.release = NULL;
   ArrowIpcInputStreamMove(input_stream, &private_data->input);
+  private_data->expected_header_prefix_size = kExpectedHeaderPrefixSizeNotSet;
 
   if (options != NULL) {
     private_data->field_index = options->field_index;