diff --git a/tests/integration/_expected_requests/debug_files/upload/chunk_upload_small_chunks.bin b/tests/integration/_expected_requests/debug_files/upload/chunk_upload_small_chunks.bin
new file mode 100644
index 0000000000..326c8b5929
Binary files /dev/null and b/tests/integration/_expected_requests/debug_files/upload/chunk_upload_small_chunks.bin differ
diff --git a/tests/integration/_responses/debug_files/assemble-chunk-upload-small-chunks.json b/tests/integration/_responses/debug_files/assemble-chunk-upload-small-chunks.json
new file mode 100644
index 0000000000..46ad1ef8e4
--- /dev/null
+++ b/tests/integration/_responses/debug_files/assemble-chunk-upload-small-chunks.json
@@ -0,0 +1,636 @@
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+      "593458e2cd88b25a750bc23a38cd9e6d5edb02ac",
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+      "2806034be3b911114fa865061f5555c1e85dbdef",
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+      "c08ade277409e2d8c32de2a71db059b2913cf45b",
+      "ffb0d4c10dc1cd10ed6f6fd732530a64b848a604",
+      "65d8818d3ccfbb504ce4ed6b5053965ab090b811",
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+      "f3d4c7238ee0dd1ffe6b625217e35b12434ad2bc",
+      "37a9bbfe0875d567af6c966fc2cc4e8e03d35601",
+      "fa0c32cd98db58a794133c268f216223a4420ea7",
+      "d77e8bc2290db760b2c0e713493e14175580b567",
+      "a779623fc005d8c08e3ad9e5c944090bf05cc724",
+      "605db3fdbaff4ba13729371ad0c4fbab3889378e",
+      "605db3fdbaff4ba13729371ad0c4fbab3889378e",
+      "605db3fdbaff4ba13729371ad0c4fbab3889378e",
+      "9cc6aecea21497009f876b268bcfb4bed415dad2",
+      "605db3fdbaff4ba13729371ad0c4fbab3889378e",
+      "605db3fdbaff4ba13729371ad0c4fbab3889378e",
+      "605db3fdbaff4ba13729371ad0c4fbab3889378e",
+      "605db3fdbaff4ba13729371ad0c4fbab3889378e",
+      "605db3fdbaff4ba13729371ad0c4fbab3889378e",
+      "605db3fdbaff4ba13729371ad0c4fbab3889378e",
+      "605db3fdbaff4ba13729371ad0c4fbab3889378e",
+      "b83ff1eacedae43641d4d8257637fd1008e6eef7",
+      "630bea217c92e8e02c3a7af7a35aa59c024a6fe9",
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+      "bd4cf063f3b470fd35a7cac722d228d92260b761",
+      "358d5763fb2019e7377bb059a9bb3ea72db910fa",
+      "b77f6cc6951b6fa515cd12e516f45505a5d58396",
+      "ba0c851ddf3a22fd15f2b7343b736a1e66be7b27",
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+      "52e2fade9aaa2407f74f3e169fd92107b23d889a",
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+      "b725c6c18dea2c19966d7e0a505161857c57003f",
+      "ad1ca3a874786dbeba87f5f142104200de70682a",
+      "a6e69a0dab96a802fd3e97a725346966a150e02a",
+      "b6378cd4bf6b23507482e535de6d609d19ca3c11",
+      "f17a710d32c1aafa7954971497a2eff119f50e55",
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+      "84fcdce8dd781653d192e077ae239c289466c770",
+      "8a91ab166ed95b79ed6ff6b12072b0c9db0346ef",
+      "41e7f0da22158c4b68b1e56af2ad8d52db94cf2c",
+      "b00341eaa95bcfabec52cc590a09dbd2068ab812",
+      "8edffe6a79caed9e07826e9d3fae11d9c177fcf6",
+      "2a30c0f2c6f51720a625eac24af75610f4a3d4b2",
+      "6fa47e7fb1ce6fbc577534740a8eb798f9bdcffc",
+      "1930ec5f11040d8c009069e456654a9363468d39",
+      "4a8b0edb116ec7c2e1f3701fbd8fedf6a50ee83b",
+      "3585c92388aedf1491f58ad40f22cc858fc3e14f",
+      "db338bfa98de9a3f166f3f44950000c23abb2ee1",
+      "29708252b0a6f8c7a5e49ee9b2701575a483e33b",
+      "59e8e46590497ccacc94282daef071e69e786f52",
+      "c2bf7c5886f28619acc2fb4cc6c979bf3684a99d",
+      "e93d4aa301859451c0d8cf5c00f1d6203251f33e",
+      "04e234bd74e9f2d0b38b07b9bf836c49502c1d9e",
+      "8fedf56abae6f72bbb71cfe24b9ab731dedc046c",
+      "1f85dfc8efbcb70d5e5de0ae46d8f31d8085ef05",
+      "ade40e7010e4f9ce419bbddcc2dcc5d5f6a9eaf6",
+      "7e5d7dcd536e9795c62a8babff6b08e91c2dd812",
+      "44bc798faa06a6d03e3ebafd1d572820be0e417e",
+      "e579a754883dea84ea547936862ff5ef8310670d",
+      "5a16069977c453be5fd8d27108707215afd52d49",
+      "531baab9c1404503f1a4855544dd25e97817a32d",
+      "6f0709626702eae2bd072b446e4b9f250a6a830d",
+      "b02acc5cf7e43e2175e6964e2725c17cf16edf27",
+      "35ff4c54da01a39779d8a47461700ef8ed4783f5",
+      "781f114ad334bcb5ea2463a9ba81398a6fcf4e38",
+      "5bc009d87ddc4aba4658f6765e6bc96a54b51cbb",
+      "051e36276c48e05b156405753c6395b1ee625db4"
+    ]
+  }
+}
diff --git a/tests/integration/_responses/debug_files/get-chunk-upload-small-chunks.json b/tests/integration/_responses/debug_files/get-chunk-upload-small-chunks.json
new file mode 100644
index 0000000000..09f7da5460
--- /dev/null
+++ b/tests/integration/_responses/debug_files/get-chunk-upload-small-chunks.json
@@ -0,0 +1,11 @@
+{
+  "url": "organizations/wat-org/chunk-upload/",
+  "chunkSize": 2048,
+  "chunksPerRequest": 64,
+  "maxFileSize": 2147483648,
+  "maxRequestSize": 33554432,
+  "concurrency": 8,
+  "hashAlgorithm": "sha1",
+  "compression": ["gzip"],
+  "accept": ["debug_files", "release_files", "pdbs", "portablepdbs", "sources", "bcsymbolmaps"]
+}
diff --git a/tests/integration/debug_files/upload.rs b/tests/integration/debug_files/upload.rs
index 8be7ee7711..ca6c00a9d7 100644
--- a/tests/integration/debug_files/upload.rs
+++ b/tests/integration/debug_files/upload.rs
@@ -1,5 +1,6 @@
+use std::collections::HashSet;
 use std::sync::atomic::{AtomicBool, Ordering};
-use std::sync::LazyLock;
+use std::sync::{Arc, LazyLock, Mutex};
 use std::{fs, str};
 
 use regex::bytes::Regex;
@@ -380,3 +381,127 @@ fn chunk_upload_multiple_files() {
         .with_default_token()
         .run_and_assert(AssertCommand::Success);
 }
+
+#[test]
+/// This test verifies a correct chunk upload of multiple debug files
+/// with a small chunk size (2048 bytes).
+/// There are also multiple requests to the chunk upload endpoint, since
+/// there are more chunk than the maximum allowed per request.
+fn chunk_upload_multiple_files_small_chunks() {
+    /// The chunk upload options specify that a single request should contain
+    /// at most 64 chunks.
+    const CHUNKS_PER_REQUEST: usize = 64;
+
+    /// 582 chunks will be uploaded in total.
+    const TOTAL_CHUNKS: usize = 582;
+
+    /// We expect the smallest number of requests that can be used to upload
+    /// all chunks, given the maximum number of chunks per request.
+    const EXPECTED_REQUESTS: usize = TOTAL_CHUNKS.div_ceil(CHUNKS_PER_REQUEST);
+
+    // Store all chunks received at the chunk upload endpoint.
+    let received_chunks = Arc::new(Mutex::new(HashSet::<Vec<_>>::new()));
+    let received_chunks_closure = received_chunks.clone();
+
+    let expected_chunks = fs::read(
+        "tests/integration/_expected_requests/debug_files/upload/chunk_upload_small_chunks.bin",
+    )
+    .expect("expected chunks file should be present");
+    // This is the boundary used in the expected request file.
+    // It was randomly generated when the expected request was recorded.
+    let expected_chunks_boundary = "------------------------au0ff4bj3Ky3LCMhImSTsy";
+
+    let is_first_assemble_call = AtomicBool::new(true);
+    TestManager::new()
+        .mock_endpoint(
+            MockEndpointBuilder::new("GET", "/api/0/organizations/wat-org/chunk-upload/")
+                .with_response_file("debug_files/get-chunk-upload-small-chunks.json"),
+        )
+        .mock_endpoint(
+            MockEndpointBuilder::new(
+                "POST",
+                "/api/0/projects/wat-org/wat-project/files/difs/assemble/",
+            )
+            .with_header_matcher("content-type", "application/json")
+            .with_response_fn(move |_| {
+                if is_first_assemble_call.swap(false, Ordering::Relaxed) {
+                    fs::read(
+                        "tests/integration/_responses/debug_files/\
+                         assemble-chunk-upload-small-chunks.json",
+                    )
+                    .expect("first assemble response file should be present")
+                } else {
+                    r#"{
+                        "6e217f035ed538d4d6c14129baad5cb52e680e74": {
+                            "state": "created",
+                            "missingChunks": []
+                        },
+                        "500848b7815119669a292f2ae1f44af11d7aa2d3": {
+                            "state": "created",
+                            "missingChunks": []
+                        },
+                        "fc27d95861d56fe16a2b66150e31652b76e8c678": {
+                            "state": "created",
+                            "missingChunks": []
+                        }
+                    }"#
+                    .into()
+                }
+            })
+            .expect(2),
+        )
+        .mock_endpoint(
+            MockEndpointBuilder::new("POST", "/api/0/organizations/wat-org/chunk-upload/")
+                .with_response_fn(move |request| {
+                    let boundary = chunk_upload::boundary_from_request(request)
+                        .expect("content-type header should be a valid multipart/form-data header");
+
+                    let body = request.body().expect("body should be readable");
+
+                    let chunks = chunk_upload::split_chunk_body(body, boundary)
+                        .expect("body should be a valid multipart/form-data body");
+
+                    // No single request should contain more than CHUNKS_PER_REQUEST chunks.
+                    assert!(chunks.len() <= CHUNKS_PER_REQUEST);
+
+                    received_chunks_closure
+                        .lock()
+                        .expect("should be able to lock mutex")
+                        .extend(chunks.into_iter().map(|chunk| chunk.into()));
+
+                    vec![]
+                })
+                .expect(EXPECTED_REQUESTS),
+        )
+        .assert_cmd(vec![
+            "debug-files",
+            "upload",
+            "tests/integration/_fixtures/debug_files/upload/chunk_upload_multiple_files",
+        ])
+        .with_default_token()
+        .run_and_assert(AssertCommand::Success);
+
+    // For simplicity, even though multiple requests are expected, the expected chunks
+    // are all stored in a single file, which was generated by setting a larger maximum
+    // number of chunks per request when generating the expected request.
+    let expected_chunks =
+        chunk_upload::split_chunk_body(&expected_chunks, expected_chunks_boundary)
+            .expect("expected chunks file should be a valid multipart/form-data body");
+
+    // Transform received chunks from a set of vectors to a set of slices.
+    let received_chunks_guard = received_chunks
+        .lock()
+        .expect("should be able to lock mutex");
+
+    let received_chunks: HashSet<_> = received_chunks_guard
+        .iter()
+        .map(|chunk| chunk.as_slice())
+        .collect();
+
+    // Use assert! because in case of failure, the output with assert_eq!
+    // is too long to be useful.
+    assert!(
+        received_chunks == expected_chunks,
+        "Uploaded chunks differ from the expected chunks"
+    );
+}