diff --git a/okhttp-tests/src/test/java/com/squareup/okhttp/internal/http/HeadersTest.java b/okhttp-tests/src/test/java/com/squareup/okhttp/internal/http/HeadersTest.java
index 6c50016bc..eef731b0a 100644
--- a/okhttp-tests/src/test/java/com/squareup/okhttp/internal/http/HeadersTest.java
+++ b/okhttp-tests/src/test/java/com/squareup/okhttp/internal/http/HeadersTest.java
@@ -21,6 +21,7 @@ import com.squareup.okhttp.Request;
 import com.squareup.okhttp.Response;
 import com.squareup.okhttp.internal.spdy.Header;
 import java.io.IOException;
+import java.util.Arrays;
 import java.util.List;
 import org.junit.Test;
 
@@ -145,6 +146,48 @@ public final class HeadersTest {
     assertEquals("OkHttp", headers.value(0));
   }
 
+  @Test public void addParsing() {
+    Headers headers = new Headers.Builder()
+        .add("foo: bar")
+        .add(" foo: baz") // Name leading whitespace is trimmed.
+        .add("foo : bak") // Name trailing whitespace is trimmed.
+        .add("ping:  pong  ") // Value whitespace is trimmed.
+        .add("kit:kat") // Space after colon is not required.
+        .build();
+    assertEquals(Arrays.asList("bar", "baz", "bak"), headers.values("foo"));
+    assertEquals(Arrays.asList("pong"), headers.values("ping"));
+    assertEquals(Arrays.asList("kat"), headers.values("kit"));
+  }
+
+  @Test public void addThrowsOnEmptyName() {
+    try {
+      new Headers.Builder().add(": bar");
+      fail();
+    } catch (IllegalArgumentException expected) {
+    }
+    try {
+      new Headers.Builder().add(" : bar");
+      fail();
+    } catch (IllegalArgumentException expected) {
+    }
+  }
+
+  @Test public void addThrowsOnNoColon() {
+    try {
+      new Headers.Builder().add("foo bar");
+      fail();
+    } catch (IllegalArgumentException expected) {
+    }
+  }
+
+  @Test public void addThrowsOnMultiColon() {
+    try {
+      new Headers.Builder().add(":status: 200 OK");
+      fail();
+    } catch (IllegalArgumentException expected) {
+    }
+  }
+
   @Test public void ofThrowsOddNumberOfHeaders() {
     try {
       Headers.of("User-Agent", "OkHttp", "Content-Length");
diff --git a/okhttp/src/main/java/com/squareup/okhttp/Cache.java b/okhttp/src/main/java/com/squareup/okhttp/Cache.java
index 04435ddd7..92a5f0bfd 100644
--- a/okhttp/src/main/java/com/squareup/okhttp/Cache.java
+++ b/okhttp/src/main/java/com/squareup/okhttp/Cache.java
@@ -485,7 +485,7 @@ public final class Cache {
         Headers.Builder varyHeadersBuilder = new Headers.Builder();
         int varyRequestHeaderLineCount = readInt(source);
         for (int i = 0; i < varyRequestHeaderLineCount; i++) {
-          varyHeadersBuilder.addLine(source.readUtf8LineStrict());
+          varyHeadersBuilder.addLenient(source.readUtf8LineStrict());
         }
         varyHeaders = varyHeadersBuilder.build();
 
@@ -496,7 +496,7 @@ public final class Cache {
         Headers.Builder responseHeadersBuilder = new Headers.Builder();
         int responseHeaderLineCount = readInt(source);
         for (int i = 0; i < responseHeaderLineCount; i++) {
-          responseHeadersBuilder.addLine(source.readUtf8LineStrict());
+          responseHeadersBuilder.addLenient(source.readUtf8LineStrict());
         }
         responseHeaders = responseHeadersBuilder.build();
 
diff --git a/okhttp/src/main/java/com/squareup/okhttp/Headers.java b/okhttp/src/main/java/com/squareup/okhttp/Headers.java
index 152f0cbde..5a5175594 100644
--- a/okhttp/src/main/java/com/squareup/okhttp/Headers.java
+++ b/okhttp/src/main/java/com/squareup/okhttp/Headers.java
@@ -171,8 +171,11 @@ public final class Headers {
   public static final class Builder {
     private final List<String> namesAndValues = new ArrayList<>(20);
 
-    /** Add an header line containing a field name, a literal colon, and a value. */
-    Builder addLine(String line) {
+    /**
+     * Add a header line without any validation. Only appropriate for headers from the remote peer
+     * or cache.
+     */
+    Builder addLenient(String line) {
       int index = line.indexOf(":", 1);
       if (index != -1) {
         return addLenient(line.substring(0, index), line.substring(index + 1));
@@ -185,6 +188,15 @@ public final class Headers {
       }
     }
 
+    /** Add an header line containing a field name, a literal colon, and a value. */
+    public Builder add(String line) {
+      int index = line.indexOf(":");
+      if (index == -1) {
+        throw new IllegalArgumentException("Unexpected header: " + line);
+      }
+      return add(line.substring(0, index).trim(), line.substring(index + 1));
+    }
+
     /** Add a field with the specified value. */
     public Builder add(String name, String value) {
       if (name == null) throw new IllegalArgumentException("name == null");
diff --git a/okhttp/src/main/java/com/squareup/okhttp/OkHttpClient.java b/okhttp/src/main/java/com/squareup/okhttp/OkHttpClient.java
index d476946da..56b55f9da 100644
--- a/okhttp/src/main/java/com/squareup/okhttp/OkHttpClient.java
+++ b/okhttp/src/main/java/com/squareup/okhttp/OkHttpClient.java
@@ -87,8 +87,8 @@ public class OkHttpClient implements Cloneable {
         return pooled.isReadable();
       }
 
-      @Override public void addLine(Headers.Builder builder, String line) {
-        builder.addLine(line);
+      @Override public void addLenient(Headers.Builder builder, String line) {
+        builder.addLenient(line);
       }
 
       @Override public void setCache(OkHttpClient client, InternalCache internalCache) {
diff --git a/okhttp/src/main/java/com/squareup/okhttp/internal/Internal.java b/okhttp/src/main/java/com/squareup/okhttp/internal/Internal.java
index 3b70b8092..d806b483c 100644
--- a/okhttp/src/main/java/com/squareup/okhttp/internal/Internal.java
+++ b/okhttp/src/main/java/com/squareup/okhttp/internal/Internal.java
@@ -52,7 +52,7 @@ public abstract class Internal {
 
   public abstract boolean isReadable(Connection pooled);
 
-  public abstract void addLine(Headers.Builder builder, String line);
+  public abstract void addLenient(Headers.Builder builder, String line);
 
   public abstract void setCache(OkHttpClient client, InternalCache internalCache);
 
diff --git a/okhttp/src/main/java/com/squareup/okhttp/internal/http/HttpConnection.java b/okhttp/src/main/java/com/squareup/okhttp/internal/http/HttpConnection.java
index a280c4e34..f78e2b635 100644
--- a/okhttp/src/main/java/com/squareup/okhttp/internal/http/HttpConnection.java
+++ b/okhttp/src/main/java/com/squareup/okhttp/internal/http/HttpConnection.java
@@ -207,7 +207,7 @@ public final class HttpConnection {
   public void readHeaders(Headers.Builder builder) throws IOException {
     // parse the result headers until the first blank line
     for (String line; (line = source.readUtf8LineStrict()).length() != 0; ) {
-      Internal.instance.addLine(builder, line);
+      Internal.instance.addLenient(builder, line);
     }
   }