diff --git a/okhttp/src/commonJvmAndroid/kotlin/okhttp3/internal/http1/HeadersReader.kt b/okhttp/src/commonJvmAndroid/kotlin/okhttp3/internal/http1/HeadersReader.kt
index 673f05329cb2..aa6ecbca05b2 100644
--- a/okhttp/src/commonJvmAndroid/kotlin/okhttp3/internal/http1/HeadersReader.kt
+++ b/okhttp/src/commonJvmAndroid/kotlin/okhttp3/internal/http1/HeadersReader.kt
@@ -15,6 +15,8 @@
  */
 package okhttp3.internal.http1
 
+import java.io.EOFException
+import java.net.ProtocolException
 import okhttp3.Headers
 import okhttp3.internal.HEADER_LIMIT
 import okio.BufferedSource
@@ -29,7 +31,23 @@ class HeadersReader(
 
   /** Read a single line counted against the header size limit. */
   fun readLine(): String {
-    val line = source.readUtf8LineStrict(headerLimit)
+    val line =
+      try {
+        source.readUtf8LineStrict(headerLimit)
+      } catch (e: EOFException) {
+        // readUtf8LineStrict() throws EOFException both when the line exceeds the byte limit
+        // and when the stream ends before a line terminator. Only the former means the response
+        // head is too large; a genuinely truncated response must still surface as an EOFException.
+        // A line of exactly headerLimit bytes is legal (okio accepts headerLimit bytes plus a
+        // terminator), so buffer.size == headerLimit is a truncated legal line, not an oversized
+        // one; only a strictly larger buffer proves the limit was exceeded.
+        if (source.buffer.size > headerLimit) {
+          throw ProtocolException(
+            "response headers exceed the ${HEADER_LIMIT / 1024} KiB limit",
+          ).initCause(e)
+        }
+        throw e
+      }
     headerLimit -= line.length.toLong()
     return line
   }
diff --git a/okhttp/src/jvmTest/kotlin/okhttp3/internal/http1/HeadersReaderTest.kt b/okhttp/src/jvmTest/kotlin/okhttp3/internal/http1/HeadersReaderTest.kt
new file mode 100644
index 000000000000..e6425e886a45
--- /dev/null
+++ b/okhttp/src/jvmTest/kotlin/okhttp3/internal/http1/HeadersReaderTest.kt
@@ -0,0 +1,80 @@
+/*
+ * Copyright (C) 2026 Square, Inc.
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License");
+ * you may not use this file except in compliance with the License.
+ * You may obtain a copy of the License at
+ *
+ *      http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS,
+ * WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+ * See the License for the specific language governing permissions and
+ * limitations under the License.
+ */
+package okhttp3.internal.http1
+
+import assertk.assertThat
+import assertk.assertions.isEqualTo
+import assertk.assertions.isInstanceOf
+import assertk.assertions.isNotNull
+import java.io.EOFException
+import java.net.ProtocolException
+import kotlin.test.assertFailsWith
+import okhttp3.internal.HEADER_LIMIT
+import okio.Buffer
+import org.junit.jupiter.api.Test
+
+class HeadersReaderTest {
+  @Test
+  fun readsNormalHeaders() {
+    val source =
+      Buffer().writeUtf8(
+        "Content-Type: text/plain\r\n" +
+          "Content-Length: 0\r\n" +
+          "\r\n",
+      )
+    val headers = HeadersReader(source).readHeaders()
+    assertThat(headers.size).isEqualTo(2)
+    assertThat(headers["Content-Type"]).isEqualTo("text/plain")
+    assertThat(headers["Content-Length"]).isEqualTo("0")
+  }
+
+  /** A header line larger than the limit reports the limit clearly instead of a raw okio dump. */
+  @Test
+  fun headerLineExceedingLimitReportsLimit() {
+    val source = Buffer().writeUtf8("a".repeat((HEADER_LIMIT + 1).toInt()))
+    val exception =
+      assertFailsWith<ProtocolException> {
+        HeadersReader(source).readHeaders()
+      }
+    assertThat(exception.message).isEqualTo("response headers exceed the ${HEADER_LIMIT / 1024} KiB limit")
+    assertThat(exception.cause).isNotNull().isInstanceOf(EOFException::class.java)
+  }
+
+  /**
+   * A response that is truncated before the limit is genuine end-of-stream, not an oversized
+   * header, so it must still surface as an [EOFException] rather than the limit message.
+   */
+  @Test
+  fun truncatedHeadersBeforeLimitStillThrowEof() {
+    val source = Buffer().writeUtf8("Content-Type: text/pl")
+    assertFailsWith<EOFException> {
+      HeadersReader(source).readHeaders()
+    }
+  }
+
+  /**
+   * A line of exactly [HEADER_LIMIT] bytes is a legal header line, so a stream that ends after that
+   * many bytes with no terminator is a truncated legal line, not an oversized header. It must still
+   * surface as an [EOFException]; the limit message is reserved for lines strictly over the limit.
+   */
+  @Test
+  fun truncatedHeadersAtLimitStillThrowEof() {
+    val source = Buffer().writeUtf8("a".repeat(HEADER_LIMIT.toInt()))
+    assertFailsWith<EOFException> {
+      HeadersReader(source).readHeaders()
+    }
+  }
+}